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.     

Revisiting the condition‐dependence of melanin‐based plumage

Support against the condition‐dependence of melanin plumage signals has relied on data from species exhibiting both melanin‐ and carotenoid‐based plumage ornaments. As the mechanisms leading to variation in carotenoid‐ and melanin‐based plumage differ fundamentally, these systems may not be ideal to assess the condition‐dependence of melanin signals. Instead, we hypothesized that melanin‐plumage is more likely to signal condition in purely achromatic species. We performed a meta‐analysis reviewing evidence for condition‐dependent melanic plumage: we compared the net effect size for the relationship between melanin traits and condition in species that are achromatic versus species that also display a carotenoid‐based trait. Our results indicate that melanin plumage is condition‐dependent in species of both plumage types. Contrarily to our prediction, this finding suggests that melanin ornament condition‐dependence is not conditional on the context of other ornaments within a species. Instead, melanin ornaments should be viewed as potential condition‐dependent signals in all species.     

Melanin, carotenoid and structural plumage ornaments: information content and role in great tits Parus major

The importance of plumage colour as an indicator of individual quality and the basis of sexual selection has long been recognized. Of the three generally distinguished classes of plumage colours, melanin-based ornaments are traditionally considered to provide less reliable information than carotenoid-based traits. However, the role of structural ornaments in multiple signalling systems has rarely been examined, and no study has compared the information content and role of the three ornament types simultaneously. Here we investigated three plumage ornaments in great tits Parus major : the size of the melanin-based breast stripe, the carotenoid-based colour of the yellow breast and the structurally based reflectance properties of the black crown. We worked on both the mechanistic and the functional levels. First, we assessed the dependence of ornaments on body condition during moult using ptilochronology. Second, we estimated assortative mating for these traits, as a measure of mutual sexual selection. Only the spectral attributes of crown feathers correlated with body condition during moult. However, breast stripe size was related to age, while the brightness of the yellow breast indicated body size. Relative crown ultraviolet reflectance was much higher in males than in females. Assortative mating was strongest for crown ultraviolet reflectance, but composite measures suggest that a system of multiple sexually selected traits with different information content may work in this population. These data support the accumulating evidence that the condition-dependence of melanin and carotenoid coloration is not qualitatively different. They also suggest that more research should target the reflectance properties of dark plumage areas in general, and ultraviolet crown ornamentation in tits in particular.     

Dorsal pattern polymorphism in female Iberian wall lizards: differences in morphology,dorsal coloration,immune response,and reproductive investment

Sex‐specific colour polymorphisms have been extensively documented in many different taxa. When polymorphism in colour pattern is restricted to females, the condition is known as female‐limited pattern polymorphism (FPP), which has been less commonly addressed in vertebrates. FPP is present in several lizard species, although most research on lizards has focused on carotenoid‐ and pteridine‐based coloration and not on melanin‐based polymorphisms. In the present study, we focus on Iberian wall lizards, Podarcis hispanicus, where two female melanin‐based dorsal patterns can be clearly distinguished: striped and reticulated‐blotched. We indirectly tested the hypothesis that selection acts differentially among P. hispanicus female morphs to create alternative morph‐specific phenotypic optima at different levels by investigating whether morphs differ in fitness proxies. We specifically examined whether the two female dorsal pattern morphs differed in adult morphology, dorsal coloration, immune response, reproductive investment, and growth. We did not find a relationship between melanin‐based coloration and hatchling growth and immune response, despite a correlation between these traits possibly being expected as a result of pleiotropy in the melanocortin system. However, our results show that female dorsal morphs in P. hispanicus differ in terms of adult morphology, dorsal coloration, and reproductive investment. Reticulated‐blotched P. hispanicus females had deeper heads and longer femora, less melanin, and more brownish coloration, and also had larger and heavier hatchlings than striped females.     

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.     

Melanin‐based coloration of sneaker male Atlantic salmon is linked to viability and emergence timing of their offspring

The ‘good genes’ hypothesis of sexual selection predicts that male ornaments are favoured by female mate choice because male ornament reveals genetic quality. In species with different male reproductive tactics, variation in genetic quality among ‘sneaking’ males has rarely been investigated, as usually ‘sneakers’ are thought not to be chosen by females. Here we focused on the alternative reproductive tactic in Atlantic salmon (Salmo salar Linnaeus, 1758) to test whether the skin colour of sneakers may reveal the performance traits of their offspring. A fully factorial breeding design was realized between 20 sneakers and two females using in vitro fertilization. We quantified the red and dark colorations of males and measured the survival of their progeny under semi‐natural conditions. In addition, the size of offspring and their emergence timing from the gravel nest were monitored in the laboratory. We found that darker males sired more viable offspring, whereas red coloration was negatively correlated with offspring survival. Nevertheless, darker and redder male pigmentations were linked to a delay in offspring emergence. These results demonstrate that colours can reveal individual genetic quality in an alternative male reproductive tactic, with male melanin‐based coloration being linked to both beneficial and detrimental effects for the offspring. Our results imply that sneaker ornaments may potentially play a role in both intra‐ and intersexual selection. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 126–135.     

Independent sources of condition dependency and multiple pathways determine a composite trait: lessons from carotenoid‐based plumage colouration

Many colour ornaments are composite traits consisting of at least four components, which themselves may be more complex, determined by independent evolutionary pathways, and potentially being under different environmental control. To date, little evidence exists that several different components of colour elaboration are condition dependent and no direct evidence exists that different ornamental components are affected by different sources of variation. For example, in carotenoid‐based plumage colouration, one of the best‐known condition‐dependent ornaments, colour elaboration stems from both condition‐dependent pigment concentration and structural components. Some environmental flexibility of these components has been suggested, but specifically which and how they are affected remains unknown. Here, we tested whether multiple colour components may be condition dependent, by using a comprehensive 3 × 2 experimental design, in which we carotenoid supplemented and immune challenged great tit nestlings (Parus major) and quantified effects on different components of colouration. Plumage colouration was affected by an interaction between carotenoid availability and immune challenge. Path analyses showed that carotenoid supplementation increased plumage saturation via feather carotenoid concentration and via mechanisms unrelated to carotenoid deposition, while immune challenge affected feather length, but not carotenoid concentration. Thus, independent condition‐dependent pathways, affected by different sources of variation, determine colour elaboration. This provides opportunities for the evolution of multiple signals within components of ornamental traits. This finding indicates that the selective forces shaping the evolution of different components of a composite trait and the trait's signal content may be more complex than believed so far, and that holistic approaches are required for drawing comprehensive evolutionary conclusions.     

Speciational evolution of coloration in the genus Carduelis

Sexual selection has been hypothesized to promote speciation, but evidence relating sexual selection to differences in speciation rates among taxa is equivocal. We note that evolutionary changes in ornaments are the link connecting sexual selection to speciation, and that ornament evolution is influenced by many factors so that its relationship with the strength of sexual selection may not be linear. We test if the evolution of ornamental coloration in Carduelis finches is related with speciation and if more ornamented lineages speciate more. We found that coloration evolves with a speciational pattern, but we found no evidence that the evolutionary changes associated with speciation are predominantly gains in ornamentation. The speciational pattern was found for both carotenoid- and melanin-based coloration, suggesting that traits putatively under stronger sexual selection by female choice (carotenoid coloration) are not the sole ones facilitating reproductive isolation. We conclude that in the genus Carduelis the evolutionary lability of ornaments influences speciation more than the strength of sexual selection, and we suggest that ornament lability should be considered as a possible causal factor in studies comparing cladogenesis among taxa.     

Temporal variation in glucocorticoid levels during the resting phase is associated in opposite way with maternal and paternal melanic coloration

Sex‐dependent selection can help maintain sexual dimorphism. When the magnitude of selection exerted on a heritable sex trait differs between the sexes, it may prevent each sex to reach its phenotypic optimum. As a consequence, the benefit of expressing a sex trait to a given value may differ between males and females favouring sex‐specific adaptations associated with different values of a sex trait. The level of metabolites regulated by genes that are under sex‐dependent selection may therefore covary with the degree of ornamentation differently in the two sexes. We investigated this prediction in the barn owl, a species in which females display on average larger black spots on the plumage than males, a heritable ornament. This melanin‐based colour trait is strongly selected in females and weakly counter‐selected in males indicating sex‐dependent selection. In nestling barn owls, we found that daily variation in baseline corticosterone levels, a key hormone that mediates life history trade‐offs, covaries with spot diameter displayed by their biological parents. When their mother displayed larger spots, nestlings had lower corticosterone levels in the morning and higher levels in the evening, whereas the opposite pattern was found with the size of paternal spots. Our study suggests a link between daily regulation of glucocorticoids and sex‐dependent selection exerted on sexually dimorphic melanin‐based ornaments.     

Phenotypic variation in nestlings of a bird of prey under contrasting breeding and diet conditions

Environmental conditions often vary in space and time, and this may explain variation in the expression of phenotypic traits related to individual quality, such as ornamental coloration. Furthermore, the direction and strength of the relationship between coloured trait expression and individual quality might vary under contrasting conditions. These issues have been explored in adult birds but much less so in nestlings, which are more likely to experience different selective pressures and different physiological trade‐offs than adults. Here, we empirically investigated the effects of contrasting breeding and diet conditions on the expression of carotenoid‐based colour traits displayed by marsh harrier (Circus aeruginosus) nestlings. We studied the variation in coloration, body condition, and immune responsiveness of nestlings in four populations over a 5‐year period. We characterized spatiotemporal differences in rearing conditions experienced by C. aeruginosus nestlings in terms of breeding (laying date, clutch size, and number of nestlings hatched and fledged) and diet (percentage of mammal in diet and prey diversity) conditions. We found that breeding conditions influenced the co‐variation between coloration and immune responsiveness in female nestlings, and that diet conditions influenced the condition‐dependence of nestling coloration in later‐hatched nestlings. In addition, breeding conditions influenced nestling body condition and immune responsiveness, whereas diet conditions influenced nestling coloration and body condition. Our study highlights that nestling phenotype (levels of signalling, circulating carotenoids, and immunity) varies both spatially and temporally, and that some of this variation is related to differences in breeding and diet conditions. Moreover, under contrasting conditions, the direction of the relationships between nestling carotenoid‐based coloration and nestling quality may also vary. In order to fully understand the evolution and maintenance of colour traits in nestling birds, studies and experiments should ideally be replicated under contrasting rearing conditions. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

The role of melanin- and carotenoid-based plumage coloration in nest defence in the Great Tit

Although plumage coloration is recognized to convey valuable information about the bearer's parental abilities, few studies have explored the relationship between coloration and nest defence. In this study in Great Tit Parus major, we analysed the relationship between nest defence and melanin‐ as well as carotenoid‐based plumage coloration, after controlling for ecological variables known to influence nest defence. A principal components analysis was applied to classify birds according to how vigorously they defended the nest, and the intensity of nest defence was tested against plumage coloration. Males with a large black tie defended their nests more vigorously, but no such effect was found for yellow breast coloration. This suggests that melanin‐based coloration in the Great Tit is associated with aggression, including both dominance‐aggression and nest defence, whereas carotenoid‐based coloration is not. The challenge in future studies will be to demonstrate whether females use this trait as an ornament to assess male quality and whether they trade off between the different ornaments a male may exhibit.     

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.     

Carotenoid ornaments and the spandrels of physiology: a critique of theory to explain condition dependency

Even as numerous studies have documented that the red and yellow coloration resulting from the deposition of carotenoids serves as an honest signal of condition, the evolution of condition dependency is contentious. The resource trade-off hypothesis proposes that condition-dependent honest signalling relies on a trade-off of resources between ornamental display and body maintenance. By this model, condition dependency can evolve through selection for a re-allocation of resources to promote ornament expression. By contrast, the index hypothesis proposes that selection focuses mate choice on carotenoid coloration that is inherently condition dependent because production of such coloration is inexorably tied to vital cellular processes. These hypotheses for the origins of condition dependency make strongly contrasting and testable predictions about ornamental traits. To assess these two models, we review the mechanisms of production of carotenoids, patterns of condition dependency involving different classes of carotenoids, and patterns of behavioural responses to carotenoid coloration. We review evidence that traits can be condition dependent without the influence of sexual selection and that novel traits can show condition-dependent expression as soon as they appear in a population, without the possibility of sexual selection. We conclude by highlighting new opportunities for studying condition-dependent signalling made possible by genetic manipulation and expression of ornamental traits in synthetic biological systems.     

Uncorrelated evolution between vocal and plumage coloration traits in the trogons: a comparative study

The costs of bird song incurred in a diversity of ways may result in trade‐offs in the production and maintenance of elaborate plumage ornaments. In this paper, we examine evolutionary trade‐offs between acoustic and visual signalling in trogon birds (Trogonidae). Using multiple regressions with phylogenetically independent contrasts, we found that interspecific variation in male plumage coloration was not significantly predicted by song traits (reduced by PCA) or altitude. Although plumage coloration is expected to decrease with increases in song elaboration, both groups of variables were not related. Given that song and plumage coloration traits are likely targets of sexual selection, we also examined their relationships with sexual plumage dimorphism. We found that male carotenoid‐derived coloration was positively related to sexual plumage dimorphism, suggesting that sexual selection on male carotenoid‐derived coloration may be stronger than on melanin‐ or structurally based coloration, or than on acoustic traits. Comparative studies on other bird families accounting for the effects of phylogeny as well as environmental covariates are required to test the generality of our findings in trogons.     

SEXUAL SELECTION,MULTIPLE MALE ORNAMENTS,AND AGE‐ AND CONDITION‐DEPENDENT SIGNALING IN THE COMMON YELLOWTHROAT

In many animals, sexual selection has resulted in complex signaling systems in which males advertise aspects of their phenotypic or genetic quality through elaborate ornamentation and display behaviors. Different ornaments might convey different information or be directed at different receivers, but they might also be redundant signals of quality that function reliably at different times (ages) or in different contexts. We explored sexual selection and age‐ and condition‐dependent signaling in the common yellowthroat (Geothlypis trichas), a sexually dichromatic warbler with two prominent plumage ornaments—a melanin‐based, black facial “mask” and carotenoid‐based, UV‐yellow “bib.” In a three‐year study, variance among males in the number of social (M_w) and extra‐pair (M_e) mates generated strong sexual selection on mask and bib attributes. Some traits (mask size, bib yellow brightness) were correlated with male age and did not experience selection beyond age‐related increases in M_w and M_e. Other traits showed age‐specific (bib size) or age‐reversed (ultraviolet brightness) patterns of selection that paralleled changes in the information‐content of each ornament. The components of male fitness generating selection in young versus old males were distinct, reflecting different sources of variation in male fertilization success. Age‐ and context‐dependent changes in the strength, direction, and target of selection may help explain the maintenance of multiple ornaments in this and other species.     

No evidence of assortative mating on the basis of putative ornamental traits in Long‐tailed Finches Poephila acuticauda

When multiple ornaments are expressed in both sexes, they are generally assumed to be maintained by mutual sexual selection and have a function in mate choice. In the Long‐tailed Finch Poephila acuticauda both sexes exhibit multiple ornaments that vary in their expression in either size (pintail and throat patch) or colour (bill) between individuals and sexes. We assessed whether these ornaments are maintained by mutual sexual selection by exploring whether individuals in a wild population paired assortatively with respect to these ornamental traits, and the degree to which the expression of these ornamental traits was indicative of reproductive success. We found no evidence of assortative pairing with respect to variation in homologous ornaments or body condition in the two sexes. In addition, we found no effect of ornament expression on the reproductive success of either males or females. Our findings suggest that the expression of these apparently ornamental traits in both sexes of this species may play no current role in mutual mate selection or as indicator traits of reproductive performance. We are currently unable to identify any function for these very elaborate ornaments in either sex of this species and suggest that the typical assumption that all such traits have an ornamental function may need further examination.     

Divergent patterns of age-dependence in ornamental and reproductive traits in the collared flycatcher

Sexual ornaments are predicted to honestly signal individual condition. We might therefore expect ornament expression to show a senescent decline, in parallel with late-life deterioration of other characters. Conversely, life-history theory predicts the reduced residual reproductive value of older individuals will favor increased investment in sexually attractive traits. Using a 25-year dataset of more than 5000 records of breeding collared flycatchers (Ficedula albicollis) of known age, we quantify cross-sectional patterns of age-dependence in ornamental plumage traits and report long-term declines in expression that mask highly significant positive age-dependency. We partition this population-level age-dependency into its between- and within-individual components and show expression of ornamental white plumage patches exhibits within-individual increases with age in both sexes, consistent with life-history theory. For males, ornament expression also covaries with life span, such that, within a cohort, ornamentation indicates survival. Finally, we compared longitudinal age-dependency of reproductive traits and ornamental traits in both sexes, to assess whether these two trait types exhibit similar age-dependency. These analyses revealed contrasting patterns: reproductive traits showed within-individual declines in late-life females consistent with senescence; ornamental traits showed the opposite pattern in both males and females. Hence, our results for both sexes suggest that age-dependent ornament expression is consistent with life-history models of optimal signaling and, unlike reproductive traits, proof against senescence.     

Brood size manipulations reveal relationships among physiological performance,body condition and plumage colour in Northern Flicker Colaptes auratus nestlings

Visual signals of quality in offspring, such as plumage colour, should honestly advertise need and/or body condition, but links between nutritional status, physiological performance and the expression of colours are complex and poorly understood. We assess how food stress during rearing affected two physiological measures (T‐cell‐mediated immune function and corticosterone level in feathers: CORT_f) and how these two variables were related to carotenoid and melanin coloration in Northern Flicker Colaptes auratus nestlings. We were also interested in how these two physiological measures were influenced by the sex of the nestling. We experimentally manipulated brood size to alter levels of food availability to nestlings during development. We measured carotenoid‐based colour (chroma and brightness) in wing feathers and the size of melanin spots on breast feathers. In agreement with our prediction, nestlings in the reduced brood treatment had better body condition and stronger immune responses than those in the control and brood enlargement treatments. This supports the hypothesis that immune responses are energetically costly. In contrast, CORT_f was not related to nestling body condition or sex and was unaffected by brood size manipulation. Nestlings of both sexes with stronger T‐cell‐mediated immune responses had larger melanin spots but only males with higher immune responses also had brighter flight feathers. Feather brightness decreased with increasing CORT_f levels. Our study is one of the few to examine the relationship between multiple physiological and plumage measures in nestlings and shows that plumage colour and immune function signalled body condition of nestlings, but that feather corticosterone levels did not.     

Multiple Plumage Ornaments as Signals of Intrasexual Communication in Golden‐Winged Warblers

Avian plumage represents some of the greatest diversity in integument coloration of all animals. Plumage signals are diverse in function, including those that allow for assessing potential mates or the mitigation of agonistic interactions between rivals. Many bird species possess multiple ornamental traits that have the potential to serve as multiple or redundant signals. For example, male golden‐winged warblers (Vermivora chrysoptera) have brilliant carotenoid‐based yellow crowns, melanin‐based black throats, and structurally based white patches on their outer tail feathers. Using a correlative approach, we investigated whether plumage ornaments have the potential to reliably signal ability to acquire higher quality territory, aggressive response to simulated territorial intrusions, and reproductive success. We found that both crown chroma and tail brightness were significantly related to habitat quality and aggression; more ornamented birds held territories with higher quality habitat and were less aggressive toward simulated conspecific stimuli. Older birds sang less threatening songs than younger birds and were more likely to sing their mate attraction song type (type 1) rather than songs typically reserved for agonistic interactions (type 2). Finally, despite our previous research demonstrating that habitat strongly predicts reproductive success in this warbler population, we found no evidence of a direct link between ornamentation and reproductive success. Overall, these data suggest that younger males, and those with lower quality ornaments, compensate with more aggressive behaviors. Additional research is needed to investigate the dynamics between behavioral traits and ornaments to better understand complex signaling and how golden wing signals function in conspecific interactions (male–male interactions and mate‐choice).     

Physiological stress links parasites to carotenoid‐based colour signals

Vertebrates commonly use carotenoid‐based traits as social signals. These can reliably advertise current nutritional status and health because carotenoids must be acquired through the diet and their allocation to ornaments is traded‐off against other self‐maintenance needs. We propose that the coloration more generally reveals an individual’s ability to cope with stressful conditions. We tested this idea by manipulating the nematode parasite infection in free‐living red grouse (Lagopus lagopus scoticus) and examining the effects on body mass, carotenoid‐based coloration of a main social signal and the amount of corticosterone deposited in feathers grown during the experiment. We show that parasites increase stress and reduce carotenoid‐based coloration, and that the impact of parasites on coloration was associated with changes in corticosterone, more than changes in body mass. Carotenoid‐based coloration appears linked to physiological stress and could therefore reveal an individual’s ability to cope with stressors.