Melanins, metals, and mate quality

Many animals display large patches of black or brown color in their integument, which contain melanin pigments and function as important sexually selected indicators of mate quality. To date, however, the particular means by which melanin-based color ornaments are costly to produce and serve as honest advertisements have remained elusive. Here, I propose a novel biochemical mechanism by which melanin-based coloration may serve as a reliable indicator of quality, involving the interplay of metal ions. In animals and other biochemical systems, a series of scarce macro- and microminerals (e.g. Ca, Zn, Cu, Fe) obtained from the diet act as critical regulatory factors in the biosynthesis of eumelanin and phaeomelanin pigments, but can also be toxic to the body when accumulated in high concentrations. As large polymers with many functional (carboxyl) groups, melanin granules also bind these metals and store them in pigmented cells. Thus, by sequestering large deposits of melanin, often in dead tissue (as in hair or feathers), animals may directly reveal dietary access to these rare elements and the physiological protection they have afforded themselves from initially beneficial, but eventually damaging, high mineral concentrations .     

Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl

Knowledge of the mechanism underlying the expression of melanin-based sex-traits may help us to understand their signalling function. Potential sources of inter-individual variation are the total amount of melanins produced but also how biochemical precursors are allocated into the eumelanin and phaeomelanin pigments responsible for black and reddish-brown colours, respectively. In the barn owl (Tyto alba), a eumelanin trait (referred to as 'plumage spottiness') signals immunocompetence towards an artificially administrated antigen and parasite resistance in females, whereas a phaeomelanin trait ('plumage coloration') signals investment in reproduction in males. This raises the question whether plumage coloration and spottiness are expressed independent of each other. To investigate this question, we have studied the genetics of these two plumage traits. Crossfostering experiments showed that, for each trait, phenotypic variation has a strong genetic component, whereas no environmental component could be detected. Plumage coloration is autosomally inherited, as suggested by the similar paternal-to-maternal contribution to offspring coloration. In contrast, plumage spottiness may be sex-linked inherited (in birds, females are heterogametic). That proposition arises from the observation that sons resembled their mother more than their father and that daughters resembled only their father. Despite plumage coloration and spottiness signalling different qualities, these two traits are not inherited independent of each other, darker birds being spottier. This suggests that the extent to which coloration and spottiness are expressed depends on the total amount of melanin produced (with more melanin leading to a both darker and spottier plumage) rather than on differential allocation of melanin into plumage coloration and spottiness (in such a case, darker birds should have been less spotted). A gene controlling the production of melanin pigments may be located on sex-chromosomes, since the phenotypic correlation between coloration and spottiness was stronger in males than in females.     

Melanin coloration in New World orioles I: carotenoid masking and pigment dichromatism in the orchard oriole complex

Carotenoids produce the brilliant red, orange, and yellow colors of many animals. However, melanin pigments can also confer some of these same hues. Because carotenoid and melanin colors are produced in different ways and may serve different signaling functions, either within or between species, it is important to establish whether one or both types of pigment are responsible for coloration. We have discovered what appears to be an evolutionary switch from carotenoid- to melanin-based color in two sexually dichromatic New World orioles. Using a combination of reflectance spectrometry and chromatographic analyses of plumage pigments, we found that the chestnut plumage of adult male orchard orioles Icterus spurius is produced predominantly by phaeomelanins. Orchard oriole feathers also contain carotenoids, which appear to be masked by the high concentration of phaeomelanins. In contrast, both carotenoids and phaeomelanins appear to contribute to color in adult male Fuertes's orioles I. fuertesi . Moreover, yellow yearling male and female plumage in both species is produced by carotenoids alone. The masking of carotenoids with phaeomelanins in orchard orioles is interesting in light of the signaling roles that carotenoids are thought to play. In addition, these plumage differences produce a unique case of age and sexual pigment dimorphism in orchard and Fuertes's orioles.     

Melanin-based plumage coloration in the house finch is unaffected by coccidial infection

For most species of birds, ornamental plumage coloration may result from two types of pigments: carotenoids and melanins. Despite the fact that melanin pigments can be synthesized by birds from basic, amino acid precursors, while carotenoids cannot be synthesized by birds and must be ingested, melanin-based plumage coloration and carotenoid-based plumage coloration have often been treated as a single trait in investigations of the function and evolution of plumage coloration. Expression of carotenoid-based coloration is known to be dependent on condition, while the effects of individual condition have not been well-tested for expression of melanin-based coloration. In this study, we experimentally tested the effect of coccidial infection of the intestinal tract of male house finches during moult on expression of melanin-based plumage coloration. Coccidial infection had a significant negative effect on carotenoid-based coloration, but it had no significant effect on melanin-based feather coloration. Unlike carotenoid-based coloration, melanin-based coloration may be cheap to produce, and honesty of melanin-based coloration my require social mediation.     

Evolution of plumage coloration in the crow family (Corvidae) with a focus on the color-producing microstructures in the feathers: a comparison of eight species

Plumage coloration has been the subject for a variety of questions that comprise the center of modern evolutionary biology. Unlike carotenoids that the concentration directly influences the intensity of the color, melanin, in addition to produce brown or black colors, is often involved in producing the structural coloration such as glossiness or iridescence. As the melanin granules can be located in the barbs or the barbules, we aim to (i) discern if the colors observed at macro scale comes from the barbs, the barbules or both in a series of related species and (ii) estimate the evolutionary history of the color-producing mechanisms in the family Corvidae that are known to have melanin-based coloration. From a preliminary comparative analysis on eight representative species, we found three coloration schemes in Corvidae; (1) matte colors of brown or black that were produced in barbs and barbules; (2) non-iridescent structural colors such as blue, bluish gray and white, that were produced in the barbs and (3) iridescent structural colors that were produced only in distal barbules. Comparative character analysis of these coloration schemes suggests that the ancestral state among these species were the colors produced in the barbs and that the color produced in the distal barbules is a derived character. The evolution of iridescence seems tightly linked to the evolution of the colors produced in the distal barbules. Data from more species should be incorporated in order to grasp a full picture on the evolutionary history of plumage coloration in this group of birds.     

Sexually selected male plumage color is testosterone dependent in a tropical passerine bird, the red-backed fairy-wren (Malurus melanocephalus)

Background

Sexual signals, such as bright plumage coloration in passerine birds, reflect individual quality, and testosterone (T) may play a critical role in maintaining signal honesty. Manipulations of T during molt have yielded mixed effects on passerine plumage color, in most cases delaying molt or leading to production of drab plumage. However, the majority of these studies have been conducted on species that undergo a post-nuptial molt when T is low; the role of T in species that acquire breeding plumage during a pre-nuptial molt remains largely unexplored.

Methodology/Principal Findings

We experimentally tested the effects of increased T on plumage color in second-year male red-backed fairy-wrens (Malurus melanocephalus), a species in which after-second-year males undergo a pre-nuptial molt into red/black (carotenoid and melanin-based) plumage and second-year males either assume red/black or brown breeding plumage. T treatment stimulated a rapid and early onset pre-nuptial molt and resulted in red/black plumage acquisition, bill darkening, and growth of the sperm storage organ, but had no effect on body condition or corticosterone concentrations. Control males molted later and assumed brown plumage. T treated males produced feathers with similar but not identical reflectance parameters to those of unmanipulated after-second-year red/black males; while reflectance spectra of red back and black crown feathers were similar, black breast feathers differed in UV chroma, hue and brightness, indicating a potentially age and plumage patch-dependent response to T for melanin- vs. carotenoid-pigmentation.

Conclusions/Significance

We show that testosterone is the primary mechanism functioning during the pre-nuptial molt to regulate intrasexually variable plumage color and breeding phenotype in male red-backed fairy-wrens. Our results suggest that the effects of T on plumage coloration may vary with timing of molt (pre- vs. post-nuptial), and that the role of T in mediating plumage signal production may differ across age classes, plumage patches, and between pigment-types.     

Why do melanin ornaments signal individual quality? Insights from metal element analysis of barn owl feathers

Melanin-based variation in colour patterns is under strong genetic control and not, or weakly, sensitive to the environment and body condition. Current signalling theory predicts that such traits may not signal honestly phenotypic quality because their production does not entail a significant fitness cost. However, recent studies revealed that in several bird species melanin-based traits covary with phenotypic attributes. In a first move to understand whether such covariations have a physiological basis, we quantified concentrations of five chemical elements in two pigmented plumage traits in the barn owl (Tyto alba). This bird shows continuous variation from immaculate to heavily marked with black spots (plumage spottiness) and from dark reddish-brown to white (plumage coloration), two traits that signal various aspects of individual quality. These two traits are sexually dimorphic with females being spottier and darker coloured than males. We found an enhancement in calcium and zinc concentration within black spots compared with the unspotted feather parts. The degree to which birds were spotted was positively correlated with calcium concentration within spots, whereas the unspotted feather parts of darker reddish-brown birds were more concentrated in zinc. This suggests that two different pigments are responsible for plumage spottiness and plumage coloration. We discuss the implications of our results in light of recent experimental field studies showing that female spottiness signals offspring humoral response towards an artificially administrated antigen, parasite resistance and fluctuating asymmetry of wing feathers.An erratum to this article can be found at     

Evidence for sexual selection on structural plumage coloration in female eastern bluebirds (Sialia sialis)

Although the function of ornamental traits in males has been the focus of intensive research for decades, expression of such traits in females has received much less study. Eastern bluebirds (Sialia sialis) display structurally based ultraviolet/blue and melanin-based chestnut plumage, and in males this plumage coloration is related to both reproductive success and competitive ability. Compared to males, female bluebirds show a subdued expression of blue and chestnut ornamental coloration, and we used a combination of an aviary nutritional-stress experiment and four years of field data to test the hypothesis that coloration functions as a signal of female quality. First, we tested the effect of food intake on expression of structural and melanin coloration in female eastern bluebirds to determine whether structural or melanin coloration are condition-dependent traits. Females that were given ad libitum access to food displayed more ornamented structural coloration than females on a food-restricted diet, but there was no effect of the experiment on melanin ornamentation. Second, we used field data to assess whether female ornamentation correlated with measures of mate quality and parental effort. The structural coloration of females predicted first egg date, maternal provisioning rates, and measures of reproductive success. These data indicate that structural coloration is dependent on nutritional condition and suggest that sexual selection is acting on structurally based plumage coloration in female eastern bluebirds.     

Structural and melanin coloration indicate parental effort and reproductive success in male eastern bluebirds

Male eastern bluebirds (Sialia sialis) have two types of ornamentalplumage coloration: a brilliant blue-ultraviolet head, back,and wings, and a patch of chestnut breast feathers. The blue-UVcoloration is produced from feather microstructure, whereasthe chestnut coloration is produced by a combination of pheaomelaninand eumelanin pigments deposited in feathers. We tested thehypothesis that plumage coloration reflects male quality ineastern bluebirds, a socially monogamous, sexually dichromaticbird. We investigated whether male ornamentation correlateswith mate quality and parental effort. We quantified three aspectsof male ornament coloration: (1) size of the patch of chestnutbreast feathers, (2) reflectance properties of the chestnutplumage coloration, and (3) reflectance properties of the blue-ultravioletplumage coloration. We found that males with larger breast patchesand brighter plumage provisioned nestlings more often, fledgedheavier offspring, and paired with females that nested earlier.Males with plumage coloration that exhibit more ultraviolethues fledged more offspring. These results suggest that plumagecoloration is a reliable indicator of male mate quality andreproductive success. Both melanin-based and structural-basedplumages appear to be honest signals of male quality and parentalcare that can be assessed by competitors or by potential mates.     

Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration

In birds, carotenoid-based plumage coloration is more dependent on physical condition and foraging abilities and less constrained developmentally than is melanin-based coloration. Thus, female mate choice for honest signals should result in more intense sexual selection on carotenoid- than on melanin-based plumage coloration. Using variation in sexual dimorphism as an indirect measure of the intensity of sexual selection, we tested the prediction mat variation in sexual dimorphism is driven more by change in carotenoid-based coloration between males and females dian by change in melanin-based coloration. Examination of historical changes in carotenoid- versus melanin-based pigmentation in 126 extant species of Cardueline finches supported this prediction. We found that carotenoid-derived coloration changed more frequendy among congeners dian melanin-based coloration. In both sexes, increase in carotenoid-based coloration score, but not in melanin-based coloration score, was strongly associated with increase in sexual dichromatism. In addition, sexual dimorphism in carotenoid-based coloration contributed more to overall dichromatism than dimorphism in melanin-based plumage. Our results supported die hypothesis that melanin-based and carotenoid-based coloration have fundamentally different signal content and suggest that combining melanin-based and carotenoid-based coloration in comparative analyses is not appropriate.     

Carotenoid-based ornamentation and status signaling in the house finch

The status signaling hypothesis (SSH) was devised primarilyto explain the adaptive significance of avian ornamental colorationduring the nonbreeding season. It proposes that conspicuousmale plumage serves as an honest signal of social status withina population of birds. However, to date this hypothesis hasbeen well tested and supported for only one type of plumage coloration, melanin-based coloration. Carotenoid-based pigmentationis known to positively reveal male health and condition duringmolt in a variety of species, but it is poorly understood whetherthis ornament type can also function as a status signal duringthe winter. We tested the SSH in male house finches (Carpodacusmexicanus) by manipulating the carotenoid-based plumage brightnessof first-year males and then pairing unfamiliar birds of differingcoloration in a series of dominance trials in captivity. Manipulated plumage color was unrelated to win/loss outcome in these trials.Similarly, the natural pigmentation of males was a poor predictorof winter dominance; as in other studies with this species,we found only a weak tendency for naturally drab males to dominatenaturally bright males. These results suggest that carotenoid-basedcoloration is not a reliable indicator of social status inmale house finches during the nonbreeding season. In fact, carotenoid-based coloration may function only in mate choice in this species,and it may be retained throughout the year either because timeconstraints preclude a second plumage molt or because it aidsin pair formation that begins in late winter.     

Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration

The striking diversity of sexual dimorphisms in nature begs the question: Why are there so many signal types? One possibility is that ornamental traits convey different sets of information about the quality of the sender to the receiver. The colourful, pigmented feathers of male birds seem to meet the predictions of this hypothesis. Evidence suggests that carotenoid pigmentation reflects the nutritional condition of males during moult, whereas in many instances melanin pigmentation is a reliable indicator of social status. However, as of yet there have been no experimental tests to determine how these two ornament types respond to the same form of environmental stress. In this study, we tested the effect of endoparasitic infection by intestinal coccidians (Isospora sp.) on the expression of both carotenoid- and melanin-based ornamental coloration in captive male American goldfinches (Carduelis tristis). We found that the carotenoid-based plumage and bill coloration of parasitized males was less saturated than that developed by unparasitized males, but that the brightness and size of melanin-based black caps did not differ between the groups. These findings provide the most robust empirical support to date for the notion that carotenoid and melanin ornaments reveal different information to conspecifics.     

Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration

Carotenoid pigments can directly enhance the immune responsesof vertebrates, and they are used by many animals to createornamental color displays. It has been hypothesized that thesetwo functions of carotenoid pigments are linked: animals musttrade off use of carotenoid pigments for immune function versusornamental display. We tested two key predictions of this hypothesiswith captive American goldfinches, Carduelis tristis, a specieswith extensive carotenoid-based plumage coloration. First, wetested whether the immune systems of male goldfinches are carotenoidlimited during molt by supplying treatment groups with low,approximately normal, or high dietary access to lutein and zeaxanthin.Dietary treatment had a significant effect on plumage and billcolor but not on immunocompetence. We compared the cell-mediatedand humoral immune responses and the course of disease afterinfection for males in the different treatments. We observedno significant effect of the carotenoid content of diet on immuneresponse or disease resistance. Second, we tested whether therewas a positive relationship between immune function and expressionof ornamental coloration by comparing both the pre- and posttreatmentplumage coloration of males to their immune responses. We failedto find the predicted trade-off between ornament display andimmune function. These findings do not support the hypothesisthat songbirds with extensive carotenoid-based plumage displaystrade off the use of carotenoids for ornamentation versus immunefunction.     

Immune and Stress Responses Covary with Melanin-Based Coloration in the Barn Swallow

Eumelanin and pheomelanin are the main endogenous pigments in animals and melanin-based coloration has multiple functions. Melanization is associated with major life-history traits, including immune and stress response, possibly because of pleiotropic effects of genes that control melanogenesis. The net effects on pheo- versus eumelanization and other life-history traits may depend on the antagonistic effects of the genes that trigger the biosynthesis of either melanin form. Covariation between melanin-based pigmentation and fitness traits enforced by pleiotropic genes has major evolutionary implications particularly for socio-sexual communication. However, evidence from non-model organisms in the wild is limited to very few species. Here, we tested the hypothesis that melanin-based coloration of barn swallow (Hirundo rustica) throat and belly feathers covaries with acquired immunity and activation of the hypothalamic–pituitary–adrenal (HPA) axis, as gauged by corticosterone plasma levels. Individuals of both sexes with darker brownish belly feathers had weaker humoral immune response, while darker males had higher circulating corticosterone levels only when parental workload was experimentally reduced. Because color of belly feathers depends on both eu- and pheomelanin, and its darkness decreases with an increase in the concentration of eu- relative to pheomelanin, these results are consistent with our expectation that relatively more eu- than pheomelanized individuals have better immune response and smaller activation of the HPA-axis. Covariation of immune and stress response arose for belly but not throat feather color, suggesting that any function of color as a signal of individual quality or of alternative life-history strategies depends on plumage region.     

Differential effects of a parasite on ornamental structures based on melanins and carotenoids

Models of sexual selection predict that ornamental colorationshould be affected by parasites in order to serve as honestsignals. Animals are commonly infested by a range of parasitespecies and often simultaneously display several ornaments.Thus the specific effect of a given parasite on ornaments isimportant for the understanding of the signal. Here we investigateexperimentally the effect of an ectoparasite on carotenoid-and melanin-based traits in breeding great tits Parus major.In the experiment, nests were either infested with hen fleas,Ceratophyllus gallinae, or kept free of parasites. The colorof the two traits and the size of the melanin-based breaststripe were assessed both in the year of experimental parasiteinfestation and during the following breeding season, afterthe annual molt. The size of the breast stripe of infested malesand females significantly decreased, but increased significantlyin uninfested males and females. The blackness of the breaststripe and the carotenoid-based plumage coloration was unaffected.Our experiment demonstrates that the size of the melanin-basedbreast stripe of adults depends on parasite infestation, suggestingthat the trait can serve as an honest signal of previous parasite exposure.     

Multiple behavioral contexts of a melanized tail display in a desert lizard

Conspicuous color displays in animals are often studied in the context of how they communicate an individual's reproductive value, ability to escape capture, or overall health. The study of sexual dichromatism often focuses on the evolution of male display traits balanced between detectability and mate acquisition, representing constraints stemming from both natural and sexual selection. Melanistic coloration and melanin color patterns play important roles in both intraspecific and interspecific signaling in animals; as melanin serves multiple purposes in organismal biology, the evolution of melanin-based visual displays might not be restricted to a single behavioral or ecological context. Here, we examine the behavioral contexts of the conspicuous melanin-based tail display in the greater earless lizard (Cophosaurus texanus), asking if this melanized tail pattern is associated with (a) female association preference of males varying in the concentration of melanin, (b) individual locomotor performance capacity, and (c) thermal ecology. We found the amount of tail melanin is linked with both locomotor performance and female association preference, with greater concentrations of melanin predicting the evolution of faster performance capacities and females preferring males with more discrete melanin bars. We found limited support that differences in melanin are linked with thermoregulation or thermal ecology. Overall, we find that multiple behavioral contexts shape the evolution of this melanized display trait. We conclude that behavioral constraints stemming from both natural and sexual selection can interact synergistically to favor the evolution and expression of a melanistic visual display, even in potentially costly ecological contexts.     

Testing whether macroevolution follows microevolution: Are colour differences among swans (<Emphasis Type="Italic">Cygnus</Emphasis>) attributable to variation at the <Emphasis Type="Italic">MC1R</Emphasis> locus?

Background  

The MC1R (melanocortin-1 receptor) locus underlies intraspecific variation in melanin-based dark plumage coloration in several unrelated birds with plumage polymorphisms. There is far less evidence for functional variants of MC1R being involved in interspecific variation, in which spurious genotype-phenotype associations arising through population history are a far greater problem than in intraspecific studies. We investigated the relationship between MC1R variation and plumage coloration in swans (Cygnus), which show extreme variation in melanic plumage phenotypes among species (white to black).     

Is male plumage reflectance correlated with paternal care in bluethroats?

Although it is now well established that the conspicuous maleplumage colors of many birds have been subject to sexual selectionby female choice, it is still debated whether females matewith colorful males to obtain direct or indirect benefits.In species where males provide substantial parental care, femalesmay obtain direct benefits from mating with the males that are best at providing care. The good parent hypothesis suggeststhat male plumage coloration signals a male's ability to provideparental care. Alternatively, the differential-allocation hypothesissuggests that colorful males reduce their care in responseto increased investment by females mated to attractive males.We tested these hypotheses on the bluethroat (Luscinia s. svecica),a socially monogamous, sexually dichromatic bird, in which males have a colorful throat patch consisting of a structurallyderived blue area surrounding a melanin-based chestnut spot.Male plumage coloration was objectively quantified by use ofreflectance spectrometry. We found no evidence of a relationshipbetween male coloration of either the blue patch or the chestnutspot and the level of paternal care. Nor were there any correlationsbetween male coloration and body size or body condition. Thus, our study does not support the hypothesis that male colorationsignals male parental quality (the good parent hypothesis)or the hypothesis that colorful males reduce their care inresponse to increased investment by females (the differential-allocationhypothesis).     

Winter Plumage Coloration in Male American Goldfinches: Do Reduced Ornaments Serve Signaling Functions in the Non‐Breeding Season?

The signaling role of sexual ornaments that are displayed during the mating season is well known for many species, but dimorphisms that occur in the non‐breeding season have received much less attention, particularly when individuals only partially express their breeding condition during reproductively inactive periods. I assessed variation in the expression of colorful breeding and non‐breeding plumages in male American goldfinches (Carduelis tristis), a species in which males molt out of their colorful breeding ornaments in the fall but still display reduced carotenoid‐ and melanin‐based sexual dichromatism during the winter. I found that variability in the saturation of carotenoid‐based plumage pigmentation did not differ significantly between the breeding and non‐breeding seasons. Moreover, the area of melanin coloration in the cap was more variable in winter than when it is fully displayed during breeding. I also detected a significant positive correlation between the extent of melanin coloration during the winter and the saturation of non‐breeding carotenoid‐based plumage. Because of such variation in and correlated expression of these two color ornaments in winter, it is conceivable that male goldfinches display these hints of non‐breeding coloration for use as conspecific social or sexual signals. Natural selection pressures like predation and energetic demands are traditionally thought of as factors that restrict sex ornaments to breeding times alone, but this should not preclude animals from simply reducing their exaggerated features during winter and finding an expression optimum that balances signal costs and value. Such ‘remnant’ winter ornaments might be expected to evolve not only in animals that live in large non‐breeding groups (e.g. status‐signaling systems) but also in those where mates begin associating before breeding onset.     

Species divergence in sexually selected traits: increase in song elaboration is related to decrease in plumage ornamentation in finches

Elaborate plumage and complex songs of male birds are two of the best-known examples of sexually selected traits, yet the interaction between these traits is poorly understood. Theory suggests that among a suite of potential displays, animals will emphasize traits that are most conspicuous, least costly, or best signal condition and reduce display of other traits. Here we examined the relationship between song and plumage elaborations in cardueline finches, songbirds that are highly variable in plumage displays and songs, but that share a similar mating system. We statistically controlled for body mass, habitat characteristics, and phylogenetic relationships and found that across species song complexity was strongly negatively related to elaboration of plumage ornamentation. When plumage coloration was partitioned into carotenoid-based and melanin-based components, song complexity was negatively related to elaboration of male carotenoid-based coloration but unrelated to elaboration of melanin-based coloration. These observations support the idea that, for condition-dependent traits, animal species trade off trait expression in response to changes in the costs or the information content of these traits. We discuss several alternative explanations for the observed pattern.