Informative content of melanin‐based plumage colour in adult Eurasian kestrels

Covariation between melanin‐based colorations and other phenotypic attributes has been rarely measured simultaneously in males and females. Such covariations and mechanisms mediating them have crucial importance determining the signalling function of these coloured ornaments in the two sexes. We examined the role of four melanin‐based coloured plumage patches as indicators of quality in both males and females of the sexually dimorphic and dichromatic Eurasian kestrel Falco tinnunculus. Previous kestrel studies have focused on the size of melanin plumage patches in either males or females as indicators of individual quality. Here, we used spectrophotometric measurements of three plumage patches and the size of another plumage patch to investigate the information content of multiple plumage colour traits in male and female kestrels. We found that females with bright plumage in the head and with high UV chroma in black parts of the rump showed good body condition and innate immunity. In addition, laying date was significantly explained by the intensity of the brown in the head of females. Meanwhile, in males we only found that individuals with greyer rumps showed better innate immunity. Altogether, our results indicate that, irrespective of the mechanism promoting covariation between coloration and individual quality, melanin‐based coloration can inform on individual quality in adult kestrels.     

Sexual selection and condition‐dependence

The handicap theory of sexual selection suggests that females prefer mates who display extravagant ornaments that advertise their quality or condition. It is often assumed that as such ornamental traits undergo sexually‐selected exaggeration, they must inevitably become more sensitive to condition, and thus more informative. Here, we show that this is not necessarily the case. Depending on the precise form of the relationship between trait size and cost, expression may become more or less condition‐dependent as the trait undergoes exaggeration, or may remain unchanged. This leads us to question how much of the information content of sexual signals can be attributed to sexual selection, and how much to pre‐existing, naturally‐selected condition‐dependence.     

Feather microstructure predicts size and colour intensity of a melanin‐based plumage signal

Feather microstructure affects the light absorbed by plumage pigments. However, the effect of particular elements of feather microstructure on the expression of pigmentary colours or on the size of colour patches has never been investigated. Here I use a model of avian visual perception and scanning electron microscope imaging of feathers to show that part of variation in the size and colour properties of a melanin‐based plumage signal of quality, the black breast stripe of great tits Parus major, is explained by three elements of feather microstructure (barbule density, barb cortex size and barb pith size). The strongest associations were between large stripes and low barbule density, between dark stripes and high barbule density, and between stripes with high relative long reflectance and high barbule density and thin barb cortex. By contrast, carotenoid‐based colour was not related to microstructural elements. Thus, it is possible that not all variation in melanin‐based colour is determined by melanin content, but also by feather microstructure. These findings should be considered by studies on the evolution of signals of quality.     

Condition‐dependence,pleiotropy and the handicap principle of sexual selection in melanin‐based colouration

The signalling function of melanin‐based colouration is debated. Sexual selection theory states that ornaments should be costly to produce, maintain, wear or display to signal quality honestly to potential mates or competitors. An increasing number of studies supports the hypothesis that the degree of melanism covaries with aspects of body condition (e.g. body mass or immunity), which has contributed to change the initial perception that melanin‐based colour ornaments entail no costs. Indeed, the expression of many (but not all) melanin‐based colour traits is weakly sensitive to the environment but strongly heritable suggesting that these colour traits are relatively cheap to produce and maintain, thus raising the question of how such colour traits could signal quality honestly. Here I review the production, maintenance and wearing/displaying costs that can generate a correlation between melanin‐based colouration and body condition, and consider other evolutionary mechanisms that can also lead to covariation between colour and body condition. Because genes controlling melanic traits can affect numerous phenotypic traits, pleiotropy could also explain a linkage between body condition and colouration. Pleiotropy may result in differently coloured individuals signalling different aspects of quality that are maintained by frequency‐dependent selection or local adaptation. Colouration may therefore not signal absolute quality to potential mates or competitors (e.g. dark males may not achieve a higher fitness than pale males); otherwise genetic variation would be rapidly depleted by directional selection. As a consequence, selection on heritable melanin‐based colouration may not always be directional, but mate choice may be conditional to environmental conditions (i.e. context‐dependent sexual selection). Despite the interest of evolutionary biologists in the adaptive value of melanin‐based colouration, its actual role in sexual selection is still poorly understood.     

Condition‐dependent expression of carotenoid‐ and melanin‐based plumage colour of northern flicker nestlings revealed by manipulation of brood size

Carotenoid‐based colouration in feathers is widely accepted to be a reliable signal of the health of an individual, but the condition‐dependence of melanin‐based plumage ornaments has been highly debated. Using broods that were manipulated in size, we tested whether nutritional stress during rearing affected the carotenoid pigmentation in secondary feathers and the size, shape, and symmetry of melanin spots on breast plumage of northern flicker Colaptes auratus nestlings. Two measures of carotenoid colour (chroma and brightness) of secondary flight feathers did not vary according to brood size treatment, but in a larger dataset from the population, carotenoid chroma was positively associated with nestling mass. Nestlings from experimentally enlarged broods had smaller melanin spots than those from reduced broods, which is some of the first experimental evidence that melanin ornament size in growing nestlings is condition‐dependent. However, the shape and symmetry of the melanin breast spots was not associated with nestling mass. Sexual dimorphism was apparent in both types of pigmentation and future studies should investigate whether there are any trade‐offs for nestlings between investing in carotenoid colouration and melanisation and whether trade‐offs differ between the sexes.     

Evolutionary shifts in the melanin‐based color system of birds

Melanin pigments contained in organelles (melanosomes) impart earthy colors to feathers. Such melanin‐based colors are distributed across birds and thought to be the ancestral color‐producing mechanism in birds. However, we have had limited data on melanin‐based color and melanosome diversity in Palaeognathae, which includes the flighted tinamous and large‐bodied, flightless ratites and is the sister taxon to all other extant birds. Here, we use scanning electron microscopy and spectrophotometry to assess melanosome morphology and quantify reflected color for 19 species within this clade. We find that brown colors in ratites are uniquely associated with elongated melanosomes nearly identical in shape to those associated with black colors. Melanosome and color diversity in large‐bodied ratites is limited relative to other birds (including flightless penguins) and smaller bodied basal maniraptoran dinosaur outgroups of Aves, whereas tinamous show a wider range of melanosome forms similar to neognaths. The repeated occurrence of novel melanosome forms in the nonmonophyletic ratites suggests that melanin‐based color tracks changes in body size, physiology, or other life history traits associated with flight loss, but not feather morphology. We further anticipate these findings will be useful for future color reconstructions in extinct species, as variation in melanosome shape may potentially be linked to a more nuanced palette of melanin‐based colors.     

Owl melanin‐based plumage redness is more frequent near than away from the equator: implications on the effect of climate change on biodiversity

Climate change acts as a major new selective agent on many organisms, particularly at high latitudes where climate change is more pronounced than at lower latitudes. Studies are required to predict which species are at a high risk of extinction and whether certain phenotypes may be more affected by climate change than others. The identification of susceptible phenotypes is important for evaluating the potential negative effect of climate change on biodiversity at the inter‐ and intraspecific levels. Melanin‐based coloration is an interesting and easily accessible candidate trait because, within certain species, reddish pheomelanin‐based coloration is associated with adaptations to warm climates. However, it is unclear whether the same holds among species. We tested one prediction of this hypothesis in four owl genera (wood, scops, screech, and pygmy owls), namely that darker reddish species are more prevalent near the equator than polewards. Our comparative analysis is consistent with this prediction for the northern hemisphere, suggesting that pale reddish species may be adapted to cold climates and dark reddish species to warmer climates. Thus, climate change may have a larger negative impact on pale pheomelanic owls and favour dark pheomelanic species. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 573–582.     

Evolution of a conspicuous melanin‐based ornament in gulls Laridae

Melanin‐ and carotenoid‐based ornaments often signal different aspects of individual quality or similar components of quality under different environmental conditions and, thus, they may become evolutionarily integrated into a composite sexual trait. On the other hand, functionally and developmentally different characters (e.g. coloration characters of different developmental origin) are more likely to evolve independently from each other than more similar traits. Here, we examined evolutionary correlations between the occurrence of a conspicuous melanin‐based ornament (hood) and carotenoid‐based bare‐part ornaments within gull family. We also aimed to identify major ecological, life‐history and biogeographical predictors of hood occurrence and reconstruct evolutionary history of this ornament. We found that hood occurrence was associated with red or dark coloration of unfeathered traits (bill and legs), whereas combinations of hood with yellow carotenoid‐based coloration of integument were evolutionarily avoided. Also, hood occurrence correlated negatively with the occurrence of other melanin‐based plumage character (mantle). Breeding latitude and habitat were identified as major predictors of hood occurrence in gulls, as hoods were recorded more frequently in low‐latitude and inland (rather than marine) species. Finally, our analysis provided support for evolutionary lability in hood occurrence, with a dominance of transitions towards hood loss in the evolutionary history of gulls. The results of our study provide one of the first evidence for a correlated evolution of melanin‐ and carotenoid‐based ornaments in an avian lineage, which supports evolutionary modularity of developmentally and functionally different coloration traits.     

Experimental stress during molt suggests the evolution of condition‐dependent and condition‐independent ornaments in the king penguin

Sexual selection and social selection are two important theories proposed for explaining the evolution of colorful ornamental traits in animals. Understanding signal honesty requires studying how environmental and physiological factors during development influence the showy nature of sexual and social ornaments. We experimentally manipulated physiological stress and immunity status during the molt in adult king penguins (Aptenodytes patagonicus), and studied the consequences of our treatments on colourful ornaments (yellow‐orange and UV beak spots and yellow‐orange auricular feather patches) known to be used in sexual and social contexts in this species. Whereas some ornamental features showed strong condition‐dependence (yellow auricular feather chroma, yellow and UV chroma of the beak), others were condition‐independent and remained highly correlated before and after the molt (auricular patch size and beak UV hue). Our study provides a rare examination of the links between ornament determinism and selection processes in the wild. We highlight the coexistence of ornaments costly to produce that may be honest signals used in mate choice, and ornaments for which honesty may be enforced by social mediation or rely on genetic constraints.     

Pro‐opiomelanocortin gene and melanin‐based colour polymorphism in a reptile

Colour polymorphism is widespread among vertebrates and plays important roles in prey–predator interactions, thermoregulation, social competition, and sexual selection. However, the genetic mechanisms involved in colour variation have been studied mainly in domestic mammals and birds, whereas information on wild animals remains scarce. Interestingly, the pro‐opiomelanocortin gene (POMC) gives rise to melanocortin hormones that trigger melanogenesis (by binding the melanocortin‐1‐receptor; Mc1r) and other physiological and behavioural functions (by binding the melanocortin receptors Mc1‐5rs). Owing to its pleiotropic effect, the POMC gene could therefore account for the numerous covariations between pigmentation and other phenotypic traits. We screened the POMC and Mc1r genes in 107 wild asp vipers (Vipera aspis) that can exhibit four discrete colour morphs (two unpatterned morphs: concolor or melanistic; two patterned morphs: blotched or lined) in a single population. Our study revealed a correlation between a single nucleotide polymorphism situated within the 3′‐untranslated region of the POMC gene and colour variation, whereas Mc1r was not found to be polymorphic. To the best of our knowledge, we disclose for the first time a relationship between a mutation at the POMC gene and coloration in a wild animal, as well as a correlation between a genetic marker and coloration in a snake species. Interestingly, similar mutations within the POMC 3′‐untranslated region are linked to human obesity and alcohol and drug dependence. Combined with our results, this suggests that the 3′‐untranslated region of the POMC gene may play a role in its regulation in distant vertebrates. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 160–168.     

Age‐ and quality‐dependent DNA methylation correlate with melanin‐based coloration in a wild bird

Secondary sexual trait expression can be influenced by fixed individual factors (such as genetic quality) as well as by dynamic factors (such as age and environmentally induced gene expression) that may be associated with variation in condition or quality. In particular, melanin‐based traits are known to relate to condition and there is a well‐characterized genetic pathway underpinning their expression. However, the mechanisms linking variable trait expression to genetic quality remain unclear. One plausible mechanism is that genetic quality could influence trait expression via differential methylation and differential gene expression. We therefore conducted a pilot study examining DNA methylation at a candidate gene (agouti‐related neuropeptide: AgRP) in the black grouse Lyrurus tetrix. We specifically tested whether CpG methylation covaries with age and multilocus heterozygosity (a proxy of genetic quality) and from there whether the expression of a melanin‐based ornament (ultraviolet‐blue chroma) correlates with DNA methylation. Consistent with expectations, we found clear evidence for age‐ and heterozygosity‐specific patterns of DNA methylation, with two CpG sites showing the greatest DNA methylation in highly heterozygous males at their peak age of reproduction. Furthermore, DNA methylation at three CpG sites was significantly positively correlated with ultraviolet‐blue chroma. Ours is the first study to our knowledge to document age‐ and quality‐dependent variation in DNA methylation and to show that dynamic sexual trait expression across the lifespan of an organism is associated with patterns of DNA methylation. Although we cannot demonstrate causality, our work provides empirical support for a mechanism that could potentially link key individual factors to variation in sexual trait expression in a wild vertebrate.     

Effect of the MC1R gene on sexual dimorphism in melanin‐based colorations

Variants of the melanocortin‐1 receptor (MC1R) gene result in abrupt, naturally selected colour morphs. These genetic variants may differentially affect sexual dimorphism if one morph is naturally selected in the two sexes but another morph is naturally or sexually selected only in one of the two sexes (e.g. to confer camouflage in reproductive females or confer mating advantage in males). Therefore, the balance between natural and sexual selections can differ between MC1R variants, as suggest studies showing interspecific correlations between sexual dimorphism and the rate of nonsynonymous vs. synonymous amino acid substitutions at the MC1R. Surprisingly, how MC1R is related to within‐species sexual dimorphism, and thereby to sex‐specific selection, has not yet been investigated. We tackled this issue in the barn owl (Tyto alba), a species showing pronounced variation in the degree of reddish pheomelanin‐based coloration and in the number and size of black feather spots. We found that a valine (V)‐to‐isoleucine (I) substitution at position 126 explains up to 30% of the variation in the three melanin‐based colour traits and in feather melanin content. Interestingly, MC1R genotypes also differed in the degree of sexual colour dimorphism, with individuals homozygous for the II MC1R variant being 2 times redder and 2.5 times less sexually dimorphic than homozygous individuals for the VV MC1R variant. These findings support that MC1R interacts with the expression of sexual dimorphism and suggest that a gene with major phenotypic effects and weakly influenced by variation in body condition can participate in sex‐specific selection processes.     

Local adaptation versus historical isolation as sources of melanin‐based coloration in the white‐throated thrush Turdus assimilis

Local adaptation seems to be one of the causes of variation in melanin‐based colors in bird plumages, related mainly to the heterogeneity of the environmental conditions along the distribution of a species. Based on comparisons of genetic (mtDNA sequences), ecological (niche models), and quantitative colorimetric data, we explored variation in plumage coloration of the white‐throated thrush Turdus assimilis, a Mesoamerican species whose dorsal color varies from brown (northern and central Mexico) to dark gray (southern Mexico and Central America). Our results suggest the existence of two major patterns of coloration in this bird, which are congruent with the genetic structure, and comparisons of ecological niche models showed that population's niches were more similar than expected by chance, suggesting that color variation in plumage of T. assimilis is not consequence of local adaptation to different environmental conditions. Our results also showed that a greater geographic distance between populations is correlated with greater colorimetric differences, suggesting that color variation in T. assimilis may be consequence of historical isolation.     

Regulation of stress response is heritable and functionally linked to melanin‐based coloration

Sexual selection theory posits that ornaments can signal the genetic quality of an individual. Eumelanin‐based coloration is such an ornament and can signal the ability to cope with a physiological stress response because the melanocortin system regulates eumelanogenesis as well as physiological stress responses. In the present article, we experimentally investigated whether the stronger stress sensitivity of light than dark eumelanic individuals stems from differential regulation of stress hormones. Our study shows that darker eumelanic barn owl nestlings have a lower corticosterone release after a stressful event, an association, which was also inherited from the mother (but not the father) to the offspring. Additionally, nestlings sired by darker eumelanic mothers more quickly reduced experimentally elevated corticosterone levels. This provides a solution as to how ornamented individuals can be more resistant to various sources of stress than drab conspecifics. Our study suggests that eumelanin‐based coloration can be a sexually selected signal of resistance to stressful events.     

Evolution of body condition‐dependent dispersal in metapopulations

Body condition‐dependent dispersal strategies are common in nature. Although it is obvious that environmental constraints may induce a positive relationship between body condition and dispersal, it is not clear whether positive body conditional dispersal strategies may evolve as a strategy in metapopulations. We have developed an individual‐based simulation model to investigate how body condition–dispersal reaction norms evolve in metapopulations that are characterized by different levels of environmental stochasticity and dispersal mortality. In the model, body condition is related to fecundity and determined either by environmental conditions during juvenile development (adult dispersal) or by those experienced by the mother (natal dispersal). Evolutionarily stable reaction norms strongly depend on metapopulation conditions: positive body condition dependency of dispersal evolved in metapopulation conditions with low levels of dispersal mortality and high levels of environmental stochasticity. Negative body condition‐dependent dispersal evolved in metapopulations with high dispersal mortality and low environmental stochasticity. The latter strategy is responsible for higher dispersal rates under kin competition when dispersal decisions are based on body condition reached at the adult life stage. The evolution of both positive and negative body condition‐dependent dispersal strategies is consequently likely in metapopulations and depends on the prevalent environmental conditions.     

Evolutionary trade‐off between naturally‐ and sexually‐selected melanin‐based colour traits in worldwide barn owls and allies

Natural selection typically constrains the evolution of sexually‐selected characters. The evolution of naturally‐ and sexually‐selected traits can be intertwined if they share part of their genetic machinery or if sex traits impair foraging success or increase the risk of depredation. The present study investigated phenotypic correlations between naturally‐ and sexually‐selected plumage traits in the Tytonidae (barn owls, grass owls, and masked owls). Phenotypic correlations indicate the extent to which selection on one trait will indirectly influence the evolution of another trait. In this group of birds, the ventral body side varies from white to dark reddish, a naturally‐selected pheomelanin‐based colour trait with important roles in predator–prey interactions. Owls also exhibit eumelanin‐based black spots, for which number and size signal different aspects of individual quality and are used in mate choice. These three plumage traits are strongly heritable and sexually dimorphic, with females being on average darker reddish and more spotted than males. Phenotypic correlations were measured between these three plumage traits in 3958 free‐living barn owls in Switzerland and 10 670 skin specimens from 34 Tyto taxa preserved in museums. Across Tyto taxa, the sexually‐selected plumage spottiness was positively correlated with the naturally‐selected reddish coloration, with redder birds being more heavily spotted. This suggests that they are genetically constrained or that natural and sexual selection are not antagonistically exerted on plumage traits. In a large sample of Swiss nestlings and within 34 Tyto taxa, the three plumage traits were positively correlated. The production of melanin pigments for one plumage trait is therefore not traded off against the production of melanin pigments for another plumage trait. Only in the most heavily‐spotted Tyto taxa do larger‐spotted individuals display fewer spots. This indicates that, at some threshold value, the evolution of many spots constrains the evolution of large spots. These analyses raise the possibility that different combinations of melanin‐based plumage traits may not be selectively equivalent.     

Seasonality of carotenoid‐based plumage coloration: modelling wavelength‐specific change through spectral reconstruction

Plumage coloration has provided important model systems for research on signal expression. Whilst it had previously been assumed that moulting provided the only mechanism to change plumage coloration, recent studies have shown plumage colours to be seasonally dynamic, with implications both for the quantification of expression and for any signalling role. However, the mechanistic processes underlying such change remain uncertain. Here, we describe within‐moult shifts in expression of a carotenoid‐based colour trait – the yellow ventral plumage of the great tit Parus major – over a nine‐month timespan. We report that plumage chromaticity (‘colour’) – but not achromaticity (‘brightness’) – exhibits a marked seasonal decline, independent of sex, age or body condition, and at a constant rate across twelve environmentally heterogeneous plots within our study site. To gain a greater understanding of the mechanisms underlying this change we employed a spectral reconstruction approach, that generates predicted spectra for any timepoint within the sampling period. By comparing spectra for both early and late in the moult we show that the seasonal decline in chromaticity is driven by both a marked reduction in ultraviolet (UV) reflectance and, to a lesser extent, loss of active carotenoid pigments. Thus, our study shows that seasonal loss of chromaticity in the great tit is driven by altered reflectance primarily in the UV section of the spectrum, a finding made possible by the use of spectral compartmentalisation and multi‐parallel modelling to produce reconstructed spectra. Whether change in plumage coloration influences signal function will depend on the dynamics of the signalling system but it could clearly inflate patterns such as assortative mating and should be considered in studies of colour expression.     

Sex‐linked inheritance,genetic correlations and sexual dimorphism in three melanin‐based colour traits in the barn owl

Theory states that genes on the sex chromosomes have stronger effects on sexual dimorphism than genes on the autosomes. Although empirical data are not necessarily consistent with this theory, this situation may prevail because the relative role of sex‐linked and autosomally inherited genes on sexual dimorphism has rarely been evaluated. We estimated the quantitative genetics of three sexually dimorphic melanin‐based traits in the barn owl (Tyto alba), in which females are on average darker reddish pheomelanic and display more and larger black eumelanic feather spots than males. The plumage traits with higher sex‐linked inheritance showed lower heritability and genetic correlations, but contrary to prediction, these traits showed less pronounced sexual dimorphism. Strong offspring sexual dimorphism primarily resulted from daughters not expressing malelike melanin‐based traits and from sons expressing femalelike traits to similar degrees as their sisters. We conclude that in the barn owl, polymorphism at autosomal genes rather than at sex‐linked genes generate variation in sexual dimorphism in melanin‐based traits.