Effects of common origin and common environment on nestling plumage coloration in the great tit (Parus major)

Abstract.— Carotenoids cannot be synthesized by birds and thus have to be ingested with food, suggesting that ca-rotenoid-based plumage coloration is environmentally determined. However signaling functions ascribed to plumage imply that plumage coloration is the outcome of an evolutionary process based on genetic variation. By means of a cross-fostering design we show significant effects of both a common rearing environment and the brood from which a nestling originally came from (common origin) on the plumage coloration of nestling great tits ( Parus major ). This demonstration of origin-related variation in carotenoid-based plumage coloration suggests that the observed variation of the trait has a partial genetic basis. Consistent with environmental determination of this trait, we also found a significant positive correlation between the color saturation of nestlings and their foster-father's plumage. There was no significant correlation between nestling plumage coloration and the food quantity provided to the nestlings by the male, the female, or both parents. This suggests that the nestling-foster father correlation arises by the carotenoid quantity ingested rather than the food quantity per se. No significant nestling-true father correlation was found, which suggests that nestling plumage coloration did not indirectly evolve due to sexual selection. Consistent with this result there was no significant correlation between the nestling's plumage color and its coloration as a breeding adult the following year, suggesting that nestling plumage color is a different trait than the first year plumage.     

Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.)

Many vertebrates use carotenoid-based signals in social or sexual interactions. Honest signalling via carotenoids implies some limitation of carotenoid-based colour expression among phenotypes in the wild, and at least five limiting proximate mechanisms have been hypothesized. Limitation may arise by carotenoid-availability, genetic constraints, body condition, parasites, or detrimental effects of carotenoids. An understanding of the relative importance of the five mechanisms is relevant in the context of natural and sexual selection acting on signal evolution. In an experimental field study with carotenoid supplementation, simultaneous cross-fostering, manipulation of brood size and ectoparasite load, we investigated the relative importance of these mechanisms for the variation in carotenoid-based coloration of nestling great tits (Parus major). Carotenoid-based plumage coloration was significantly related to genetic origin of nestlings, and was enhanced both in carotenoid-supplemented nestlings, and nestlings raised in reduced broods. We found a tendency for ectoparasite-induced limitation of colour expression and no evidence for detrimental effects of carotenoids on growth pattern, mortality and recruitment of nestlings to the local breeding population. Thus, three of the five proposed mechanisms can generate individual variation in the expression of carotenoid-based plumage coloration in the wild and thus could maintain honesty in a trait potentially used for signalling of individual quality.     

Body condition variation in kestrel (<Emphasis Type="Italic">Falco tinnunculus</Emphasis>) nestlings in relation to breeding conditions

The body condition index (i.e., body mass corrected for age or size differences) is commonly used to investigate offspring condition in nestling birds. The body condition index reflects different parameters related to the general nutritional state of nestlings and may predict survival prospects. Since conditions experienced during the growth period can affect the fitness of nestlings in adulthood, we investigated proximate and ultimate factors underlying body condition index variation in kestrel (Falco tinnunculus) nestlings in a 9-year field study and we carried out two cross-fostering experiments to disentangle the origin (genetics plus maternal effects) and rearing (environment effect) components of body condition index variation. In total, we sampled 2,065 nestlings from 464 broods and used 121 nestlings from 24 broods in the cross-fostering experiments. We found that nestlings from larger broods had higher body condition index than nestlings from smaller ones, but this pattern did not emerge in two of the 9 years of study; nestlings born later in the breeding season had lower body condition index in some years but not in others; the decrease of body condition index over the breeding season emerged in all but three-chick broods; males and females did not differ neither in body condition index nor in the covariation between body mass and wing length, while this result was limited to one of the nine field study years; the annual mean value of body condition index did not covary with the total rainfall; both the origin and rearing components explained body condition index variation, but their relative contributions varied from a year to another. Overall, these results suggest that the brood size is not a good predictor of body condition index; the rule “nesting early in the season is better” is less general than previously thought; the body condition index may contain origin variance, whose expression may be modulated by environmental conditions.     

Effects of nestling condition on UV plumage traits in blue tits: an experimental approach

Intraspecific sexual and social communications are among themost important factors shaping costly color traits in birds.Condition capture models assume that only animals in superiorcondition can develop and maintain a colorful plumage. Althoughthere is good evidence that carotenoid-based components of plumagecolors show condition dependence, the situation is more controversialwith the underlying UV-reflecting structural component. We conducteda brood size manipulation in blue tits (Parus caeruleus) toinvestigate condition-dependent effects on plumage colorationin male and female offspring. Carotenoid chroma and UV reflectanceof the yellow breast plumage showed condition-dependent expressionin male and female fledglings. However, only males that wereraised in reduced broods had higher UV reflectance in the UV/bluetail feathers, whereas female tail coloration did not differbetween treatments. Our data suggest that there is a sex-specificeffect on the blue but not the yellow plumage and that thisis related to differences in the signaling function of bothplumage traits. Although sexual selection may already act onmale nestlings to develop colorful tail feathers for the nextbreeding season, the UV/yellow breast feathers are molted duringthe postjuvenile molt, and their signaling value is likely tobe important for both sexes during the extended postfledglingphase.     

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     

Developmental plasticity varied with sex and position in hatching hierarchy in nestlings of the asynchronous European roller,Coracias garrulus

Allocation rules between ornamental and other functional traits of birds may differ among individuals and vary with environmental conditions. We supplemented roller (Coracias garrulus) nestlings with methionine in a between‐nest design to investigate the way in which the sex and position in the hatching hierarchy affect the allocation of resources among growth, immunity, and plumage coloration. Methionine induces the production of lymphocytes at expense of growth; thus, we used it to manipulate growth and immunity, which are two traits likely to compromise plumage coloration. We predicted that late‐hatched chicks within a brood (juniors) compared to early‐hatched chicks (seniors) should allocate more to traits directly providing fitness than to ornamental traits because juniors are more affected than seniors by sibling competition. The methionine treatment effectively enhanced the production of lymphocytes in experimental broods. This appeared to be at the expense of plumage coloration in junior nestlings because, in supplemented nests, junior males showed a trend to display less greenish bellies than junior males from control nests. However, juniors from supplemented nests maintained wing growth as in control juniors. The plumage coloration of seniors was unaffected by the methionine supplementation, although they paid the costs of lymphocyte production at a level of growth that was reduced compared to senior nestlings in control nests. Hence, sex, and hatching order affected resource allocation among growth, immunity, and plumage coloration of roller nestlings. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 500–511.     

No evidence for survival selection on carotenoid-based nestling coloration in great tits (Parus major)

In several vertebrate species evidence supports the hypothesis that carotenoid-based coloration of adults has evolved due to sexual selection. However, in some birds already the nestlings display carotenoid-based coloration. Because the nestling's body plumage is typically moulted before the first reproductive event, sexual selection cannot explain the evolution of these carotenoid-based traits. This suggests that natural selection might be the reason for its evolution. Here we test whether the carotenoid-based nestling coloration of great tits (Parus major) predicts survival after fledging. Contrary to our expectation, the carotenoid-based plumage coloration was not related to short- nor to long-term survival in the studied population. Additionally, no prefledging selection was detectable in an earlier study. This indicates that the carotenoid-based coloration of nestling great tits is currently not under natural selection and it suggests that past selection pressures or selection acting on correlated traits may have led to its evolution.     

Sex-specific development of cell-mediated immunity under experimentally altered rearing conditions in blue tit nestlings

In birds, poor rearing conditions usually have negative effects on T-cell-mediated immune response. However, earlier studies demonstrate that fitness-related traits such as body mass may show sex-specific patterns when subject to alteration of rearing conditions. Therefore, to investigate whether deterioration of rearing conditions influences the development of immune function differently in male and female nestlings, we performed brood size manipulation experiments on blue tit (Parus caeruleus) nestlings. To alter rearing conditions, some broods were increased by three nestlings soon after hatching, while other broods were left non-manipulated. Immune response was assessed as a hypersensitivity reaction to phytohaemagglutinin in 11-day-old nestlings. Additionally, we studied the consequences of brood size manipulation for fledgling body mass and tarsus length. The enlargement of brood size had different effects on the cellular immune responses of male and female nestlings, with males being more negatively affected than their female nest-mates. Sex-specific effects of poor rearing conditions were also recorded for tarsus length, such that tarsus growth was more retarded in female than in male nestlings. We discuss the effects of deterioration of rearing conditions on sex-specific development of cell-mediated immunity with respect to sexual dimorphism of size and developmental strategies in male and female nestlings.     

Females mate with males with diminished pheomelanin‐based coloration in the Eurasian nuthatch Sitta europaea

Sexual selection can drive the evolution of phenotypic traits because of female preferences for exaggerated trait expression in males. Sexual selection can also lead to the evolutionary loss of traits, a process to which female preferences for diminished male trait expression are hypothesized to contribute. However, empirical evidence of female preferences for diminished male traits is virtually lacking. Eurasian nuthatches Sitta europaea provide an opportunity to test this possibility, as a chestnut flank patch produced by the pigment pheomelanin is present since the first plumage of these birds and its color is more intense in nestlings in poor condition in our study population. It has been proposed that developing birds in poor condition may increase their production of pheomelanin as a detoxifying strategy. Female nuthatches may thus prefer mating with males showing flank feathers of diminished color, as this could indicate that males experienced good conditions early in development, which can positively affect the fitness of future generations. Here we show results according with this prediction in a wild population of Eurasian nuthatches, as adult males with lighter chestnut feathers paired earlier in the season, while chestnut coloration had no effect on female mating success. Chestnut color expression was not affected by the body condition of birds, suggesting that females obtain information on the body condition in early life of their potential mates and not on their current body condition. This constitutes one of the few examples of females mating with males showing diminished traits and provides the only explanation so far by which this process can occur.     

The influence of environmental conditions on immune responses, morphology and recapture probability of nestling house martins (Delichon urbica)

Nestling birds produced later in the season are hypothesized to be of poor quality with a low probability of survival and recruitment. In a Spanish population of house martins (Delichon urbica), we first compared reproductive success, immune responses and morphological traits between the first and the second broods. Second, we investigated the effects of an ectoparasite treatment and breeding date on the recapture rate the following year. Due probably to a reverse situation in weather conditions during the experiment, with more rain during rearing of the first brood, nestlings reared during the second brood were in better condition and had stronger immune responses compared with nestlings from the first brood. Contrary to other findings on house martins, we found a similar recapture rate for chicks reared during the first and the second brood. Furthermore, ectoparasitic house martin bugs had no significant effect on the recapture rate. Recaptured birds had similar morphology but higher immunoglobulin levels when nestlings compared with non-recaptured birds. This result implies that a measure of immune function is a better predictor of survival than body condition per se.     

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.     

Extra-pair paternity, testes size and testosterone level in relation to colour polymorphism in the barn owl Tyto alba

In many bird populations, individuals display one of several genetically inherited colour morphs. Colour polymorphism can be maintained by several mechanisms one of which being frequency-dependent selection with colour morphs signalling alternative mating strategies. One morph may be dominant and territorial, and another one adopt a sneaky behaviour to gain access to fertile females. We tested this hypothesis in the barn owl Tyto alba in which coloration varies from reddish-brown to white. This trait is heritable and neither sensitive to the environment in which individuals live nor to body condition. In Switzerland, reddish-brown males were observed to feed their brood at a higher rate and to produce more offspring than white males. This observation lead us to hypothesize that white males may equalise fitness by investing more effort in extra-pair copulations. This hypothesis predicts that lighter coloured males produce more extra-pair young, have larger testes and higher levels of circulating testosterone. However, our results are not consistent with these three predictions. First, paternity analyses of 54 broods with a total of 211 offspring revealed that only one young was not sired by the male that was feeding it. Second, testes size was not correlated with male plumage coloration suggesting that white males are not sexually more active. Finally, in nestlings at the time of feather growth testosterone level was not related to plumage coloration suggesting that this androgen is not required for the expression of this plumage trait. Our study therefore indicates that in the barn owl colour polymorphism plays no role in the probability of producing extra-pair young.     

Plumage colour in nestling blue tits: sexual dichromatism,condition dependence and genetic effects

Sexual-selection theory assumes that there are costs associated with ornamental plumage coloration. While pigment-based ornaments have repeatedly been shown to be condition dependent, this has been more difficult to demonstrate for structural colours. We present evidence for condition dependence of both types of plumage colour in nestling blue tits (Parus caeruleus). Using reflectance spectrometry, we show that blue tit nestlings are sexually dichromatic, with males having more chromatic (more 'saturated') and ultraviolet (UV)-shifted tail coloration and more chromatic yellow breast coloration. The sexual dimorphism in nestling tail coloration is qualitatively similar to that of chick-feeding adults from the same population. By contrast, the breast plumage of adult birds is not sexually dichromatic in terms of chroma. In nestlings, the chroma of both tail and breast feathers is positively associated with condition (body mass on day 14). The UV/blue hue of the tail feathers is influenced by paternally inherited genes, as indicated by a maternal half-sibling comparison. We conclude that the expression of both carotenoid-based and structural coloration seems to be condition dependent in blue tit nestlings, and that there are additional genetic effects on the hue of the UV/blue tail feathers. The signalling or other functions of sexual dichromatism in nestlings remain obscure. Our study shows that nestling blue tits are suitable model organisms for the study of ontogenetic costs and heritability of both carotenoid-based and structural colour in birds.     

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.     

A melanin-based trait reflects environmental growth conditions of nestling male Eurasian kestrels

Melanin pigments are responsible for most non-structural brown, black and grey colouration in animals. The extent to which melanin-based colouration in birds is genetically or environmentally determined has been subject to controversy. One reason for this it is paucity of empirical data on the role of key environmental factors, such as food availability, on the development of melanin-based traits. We analysed whether brown and grey colouration in rumps of Eurasian kestrels Falco tinnunculus is based on melanin and examined the relationships between high inter-annual variation in main food supply, parental condition and the expression of grey colouration in male nestlings. We also performed a partial cross-fostering experiment to allocate randomly nestlings among environments. The proportion of male nestlings with predominantly grey colouration was higher in years with abundant prey (voles). The only variable associated with intra-annual variation of grey colouration in male nestlings was body mass of the female rearing them. The colouration of nestlings in the cross-foster experiment was correlated with the body mass of their foster mother, but not with that of their genetic mother. Melanin colouration did not correlate with T-cell mediated immune response. These results indicate that this melanin-based trait reflects the environmental conditions in which the nestlings grew up.     

Genetic and environmental variation in immune response of collared flycatcher nestlings

This paper aims at partitioning genetic and environmental contribution to the phenotypic variance in nestling immune function measured with the hypersensitivity test after inoculation with phytohaemagglutinin. A cross-fostering experiment with artificial enlargement of some broods was conducted. Variation in nestling immune response was related to their common origin, which suggests heritable component of cell-mediated immunity. A common rearing environment also explained a significant part of variation. However, deterioration of rearing conditions as simulated by enlargement of brood size did not affect nestling immunocompetence, although it affected nestling body mass. Variation in body mass explained some of the variation in immune response related to rearing environment, which means that growth is more sensitive to the shifts in rearing conditions than the development of immune function. Heritable variation in immune response suggests that there should be potential for selection to operate and the micro evolutionary changes in immunity of flycatcher nestlings are possible.     

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.     

Geographic variation in sexual dimorphism in the barn owl Tyto alba: a role for direct selection or genetic correlation?

Geographic variation in sexually selected traits is commonly attributed to geographic variation in the net benefit accrued from bearing such traits. Although natural and sexual selection are potentially important in shaping geographic variation, genetic constraints may also play a role. Although a genetic correlation between two traits may itself be the outcome of natural or sexual selection, it may indirectly reinforce the establishment and maintenance of cline variation with respect to one particular trait when across the cline different values of other traits are selected. Using the barn owl Tyto alba, a species in which the plumage of females is more reddish‐brown and more marked with black spots than that of males, I report results that are consistent with the hypothesis that both direct selection and genetic constraints may help establish and maintain cline variation in sexual dichromatism. In this species, inter‐individual variation in plumage coloration and spottiness has a genetic basis, and these traits are not sensitive to the environment. Data, based on the measurement of skin specimens, is consistent with the hypothesis that the stronger European cline variation in male spottiness than in female spottiness depends on the combined effects of (1) the similar cline variation in male and female plumage coloration and (2) the more intense phenotypic correlation between plumage coloration and spottiness in males (darker birds are more heavily spotted in the two sexes, but especially males) which is a general feature among the globally distributed barn owls. In northern Europe, male and female T. a. guttata are reddish‐brown and heavily spotted, and in southern Europe male and female T. a. alba are white, but only females display many spots. Here, I discuss the relative importance of direct selection, genetic correlation and the post‐ice age invasion of Europe by T. alba, in generating sex‐specific cline variation in plumage spottiness and non‐sex‐specific cline variation in plumage coloration.     

Environmental and Parental Influences on Offspring Health and Growth in Great Tits (Parus major)

Sexual selection requires both that there is heritable variation in traits related to fitness, and that either some of this variation is linked to traits of the parents, and/or that there are direct benefits of choosing particular individuals as mates. This suggests that if direct benefits are important offspring performance should be predicted by traits of the rearing adults. But if indirect benefits are more significant offspring performance should be predicted by traits of the adults at the nest-of-origin. We conducted cross-fostering experiments in great tits (Parus major) over four years, in two of which we manipulated environmental conditions by providing supplemental food. In a third year, some nestlings were directly supplemented with carotenoids. Nestlings in broods whose rearing adults received supplemental food were heavier and had improved immune responses even when controlling for body mass. Nestling immune function was related to measures of the yellow plumage color of both the rearing male and the putative father. Nestling body mass was influenced by the coloration of both the rearing female and the genetic mother. Our results suggest that features of both their social and putative genetic parents influence nestling health and growth. From this it would appear that females could be gaining both direct and indirect benefits through mate choice of male plumage traits and that it would be possible for males to similarly gain through mate choice of female traits.     

Cross‐fostering reveals that among‐brood differences in ornamental mouth coloration mostly reflect rearing conditions in nestling house sparrows

Dependent offspring use specialized traits to attract parental care. In birds, this includes morphological ornaments (e.g. colourful plumage or mouthparts) that are associated with nestling condition and shape the allocation of parental care. Ornament expression often differs among broods, even after differences in individual condition are accounted for statistically. Understanding how this variation arises is important for understanding the information content of these signals, their functional importance, and their evolution. The present study used a cross‐fostering experiment to assess the relative contributions of parental effects to among‐brood differences in the mouth coloration of nestling house sparrows, specifically the carotenoid‐richness, overall brightness, and ultraviolet (UV) coloration of rictal flanges. The expression of carotenoid‐based coloration was explained by synchronous breeding, nest‐of‐rearing and nest‐of‐origin. Brightness and relative UV intensity, however, were explained only by synchronous breeding, and there was substantial unexplained variation in all three colour parameters. Among‐brood variation in mouth coloration, then, may primarily contain information about the environment in which offspring are reared. At the individual level, ontogenetic changes in the carotenoid‐richness and brightness of flanges positively reflected mass gain (a proxy for food intake). Larger and yellower chicks gained more mass, consistent with parental preferences for these traits. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 169–179.