Age differences in blue tit Parus caeruleus plumage colour: within‐individual changes or colour‐biased survival?

In many species of passerine birds yearlings display a less elaborate version of the adult secondary sexual traits, but the causes of such differences in ornamentation are not always well understood. We studied age-related changes in blue tit Parus caeruleus UV/blue structural crown coloration, a sexually selected trait. In our Austrian study population, older blue tits, irrespective of sex, displayed on average a more ultraviolet (lower hue, higher UV chroma), more chromatic and brighter crown coloration than yearlings. This age dichromatism was caused by within-individual changes in the expression of crown coloration between years since males and females became more UV, more chromatic and brighter as they aged. Colour biased survival did not contribute to the observed pattern of age dichromatism since crown coloration was largely unrelated to overwinter survival. Between-year repeatability of crown colour was significant for most colour variables but low in general, and lower for females than for males. In the blue tit, yearling males might benefit from being less ornamented by avoiding adult aggression but at the expense of sexual attractiveness. Adaptive explanations of blue tit age dichromatism should however take into account that age effects were of similar magnitude in males and females. This suggests that both male and female yearlings could benefit from being less ornamented and hence that sexual selection might be acting on both sexes simultaneously in this species.     

No evidence for general condition-dependence of structural plumage colour in blue tits: an experiment

Condition-dependence is a central but contentious tenet of evolutionary theories on the maintenance of ornamental traits, and this is particularly true for structural plumage colour. By providing diets of different nutritional quality to moulting male and female blue tits, we experimentally manipulated general condition within the natural range, avoiding deprivation or stressful treatments. We measured reflectance of the structural-coloured UV/blue crown, a sexually selected trait in males, and the white cheek, a nonpigmented structural colour, directly after moult and again during the following spring mating season. We employed a variety of colour indices, based on spectral shape and avian visual models but, despite significant variation in condition and coloration, found no evidence for condition-dependence of UV/blue or white plumage colour during either season. These and previously published results suggest that structural colour might be sensitive to stress, rather than reduced body condition, during moult.     

Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus)

In socially monogamous species, extra-pair paternity can increase the variance in reproductive success and thereby the potential for sexual selection on male ornaments. We studied whether male secondary sexual ornaments are selected through within- and/or extra-pair reproductive success in the blue tit (Parus caeruleus). Male blue tits display a bright blue crown plumage, which reflects substantially in the ultraviolet (UV) and previously has been indicated to be an important sexual signal. We show that males with a more UV-shifted crown hue were less cuckolded, which probably resulted from female preference for more ornamented mates. By contrast, however, older males and males with a less UV-shifted hue sired more extra-pair young. This probably did not reflect direct female preference, since cuckolders were not less UV-ornamented than the males they cuckolded. Alternatively, a trade-off between UV ornamentation and other traits that enhance extra-pair success could explain this pattern. Our results might reflect two alternative male mating tactics, where more UV-ornamented males maximize within-pair success and less UV-ornamented males maximize extra-pair success. Since crown colour was selected in opposite directions by within-pair and extra-pair paternity, directional selection through extra-pair matings seemed weak, at least in this population and breeding season. Reduced intensity of sexual selection due to alternative mating tactics constitutes a potential mechanism maintaining additive genetic variance of male ornaments.     

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.     

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.     

Concordant evolution of plumage colour, feather microstructure and a melanocortin receptor gene between mainland and island populations of a fairy-wren

Studies of the patterns of diversification of birds on islands have contributed a great deal to the development of evolutionary theory. In white-winged fairy-wrens, Malurus leucopterus, mainland males develop a striking blue nuptial plumage whereas those on nearby islands develop black nuptial plumage. We explore the proximate basis for this divergence by combining microstructural feather analysis with an investigation of genetic variation at the melanocortin-1 receptor locus (MC1R). Fourier analysis revealed that the medullary keratin matrix (spongy layer) of the feather barbs of blue males was ordered at the appropriate nanoscale to produce the observed blue colour by coherent light scattering. Surprisingly, the feather barbs of black males also contained a spongy layer that could produce a similar blue colour. However, black males had more melanin in their barbs than blue males, and this melanin may effectively mask any structural colour produced by the spongy layer. Moreover, the presence of this spongy layer suggests that black island males evolved from a blue-plumaged ancestor. We also document concordant patterns of variation at the MC1R locus, as five amino acid substitutions were perfectly associated with the divergent blue and black plumage phenotypes. Thus, with the possible involvement of a melanocortin receptor locus, increased melanin density may mask the blue-producing microstructure in black island males, resulting in the divergence of plumage coloration between mainland and island white-winged fairy-wrens. Such mechanisms may also be responsible for plumage colour diversity across broader geographical and evolutionary scales.     

The effects of environmental heterogeneity on multivariate selection on reproductive traits in female great tits

Describing natural selection on phenotypic traits under varying environmental conditions is essential for a quantitative assessment of the scale at which adaptation might occur and of the impact of environmental variability on evolution. Here we analyzed patterns of multivariate selection via fecundity and viability on three reproductive traits (laying date, clutch size, and egg weight) in a population of great tits (Parus major). We quantified selection under different environmental conditions using (1) local variation in breeding density and (2) distinct areas of the population's habitat. We found that selection gradients were generally stronger for fecundity than for viability selection. We also found correlational selection acting on the combination of laying date and clutch size; this is the first documented evidence of such selection acting on these two traits in a passerine bird. Our analyses showed that both local breeding density and habitat significantly influenced selection patterns, hence favoring different patterns of reproductive investment at a small-scale relative to typical dispersal distances in this species. Canonical rotation of the nonlinear selection matrices yielded similar conclusions as traditional nonlinear selection analyses, and also showed that the main axes of selection and fitness surfaces varied over space within the population. Our results emphasize the importance of quantifying different forms of selection, and of including variation in environmental conditions at small scales to gain a better understanding of potential evolutionary dynamics in wild populations. This study suggests that the fitness landscape for this species is relatively rugged at scales relevant to the life histories of individual birds and their close relatives.     

Seasonal changes in a ultraviolet structural colour signal in blue tits, Parus caeruleus

Recent studies of blue tits, Parus caeruleus , have found sexual selection and a viability-indicating function of the structural ultraviolet and blue crown plumage, but the reasons for this signal variation are not understood. Furthermore, studies in England and Sweden have yielded somewhat different results (particularly with regard to the spectral position of the reflectance peak). Here we investigate whether the blue tit UV/blue ornament varies with time of year since such variation might be relevant to the signalling function as well as the apparent difference between populations. From 400 blue tits captured at two different localities in Sweden, we found that objective measures of 'hue' (spectral location), 'chroma' (spectral purity) and 'brightness' (spectral intensity), varied substantially with season. Just after moult (October), crown 'hue' is maximally UV-shifted (359 nm for males and 373 nm for females). Thereafter the peak drifts upwards and by the time of nestling feeding (June) male reflectance peaks at 404 nm and female at 413 nm. This change is probably due to feather wear as well as fat and dirt accumulation, which might constitute an additional male quality cue. Our results suggest that it is important to consider plumage age when exploring variation in structural plumage coloration, and that it can largely explain the difference between the British and Swedish studies. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 237–245.     

Ultraviolet reflectance affects male-male interactions in the blue tit (Parus caeruleus ultramarinus)

Several animal species have been shown to use phenotypic traitsto assess the competitive ability of opponents and adjust theiraggressiveness depending on the likelihood to win the contest.In birds, these phenotypic traits usually involve patches ofcolored feathers. The benefit to harbor honest signals of malequality is the avoidance of wasteful aggressive interactions.Recent work has shown that ultraviolet (UV) plumage reflectanceis an important signal used by females during mate choice. Surprisingly,however, the role of UV signaling on intrasexual selection hasbeen neglected. In the present study, we aimed to test whetherUV reflectance of crown feathers was used as a signal of malecompetitive ability during male-male interactions. Breedingmale blue tits (Parus caeruleus ultramarinus) were exposed duringthe female egg-laying period to blue tit taxidermic mounts witheither control or reduced UV reflectance of crown feathers.In agreement with the prediction that UV reflectance advertisesmale quality, we found that breeding blue tits behaved lessaggressively toward the UV-reduced decoy. To our knowledge,this is the first experimental evidence suggesting a role forUV signaling on intrasexual selection.     

Structural plumage colour and parasites in satin bowerbirds Ptilonorhynchus violaceus: implications for sexual selection

We investigated whether variation in structural plumage coloration in satin bowerbirds, Ptilonorhynchus violaceus , could reveal the intensity of infection from parasites, as predicted from models of parasite-mediated sexual selection (PMSS). To do this, we captured adult male, female, and juvenile male satin bowerbirds in Queensland, Australia, and objectively measured individual plumage reflectance from four body regions using a spectrometer. We quantified both ectoparasite load and the intensity of infection from blood parasites. In iridescent blue adult males, plumage reflectance is unimodal, with a single peak in the ultraviolet, while in greenish females and juveniles, plumage reflectance is bimodal, with peaks in both the ultraviolet and green portions of the spectrum. In adult males, the intensity of infection from blood parasites was best predicted by plumage brightness (total reflectance), with brighter males having fewer parasites. Similarly, juvenile males exhibiting greater UV chroma (proportion of reflectance in the UV) had fewer blood parasites. Our findings support a key prediction of PMSS models and provide the first evidence that a structural colour ornament can signal the intensity of infection from blood parasites.     

Plumage color as a status signal in male–male interaction in the red-flanked bushrobin, Tarsiger cyanurus

Recent studies have suggested that structural-based coloration is an honest signal of male genetic and/or conditional quality in sexual selection. However, whether structural coloration functions in intrasexual competition is unknown. We examined whether plumage color functions as a status signal during intrasexual interactions in the red-flanked bushrobin Tarsiger cyanurus; adult males have many blue plumes as structural coloration whereas yearling males and females are olive brown with few blue plumages. Blue males did not always dominate olive-brown males. The number of interactions did not differ with the colors of the two birds involved. The interactions of a blue male and an olive-brown male were less aggressive than those of two blue or of two olive-brown males. In this study, we found that structural plumage coloration may serve as a signal of aggressive intent and lower the escalation level of an aggressive interaction in a manner consistent with hypotheses regarding the evolution of delayed plumage maturation.     

Territorial responses of male blue tits, Cyanistes caeruleus , to UV-manipulated neighbours

Multiple phenotypic traits can affect the outcome of interactions among territorial animals. Individuals may use current and previously acquired information on phenotypic traits to assess the competitive ability of opponents and adjust the strength of their response depending on the threat the opponent poses. In birds, colourful plumage and song are widespread phenotypic traits. Recent work has shown that ultraviolet (UV) plumage reflectance may be used by males in assessing an opponent’s strength and by females in mate choice. In the present study, we investigated whether and how territorial male blue tits, Cyanistes caeruleus, use previously acquired information from UV reflectance of the crown feathers of neighbours to adjust their response to playback of song of these neighbours simulated to intrude their territory. We compared responses to neighbours with those to unfamiliar strangers with unknown plumage features. We found that subject males with UV-enhanced neighbours responded more strongly to these neighbours than to strangers, i.e. showed more flights, used songs without trill and tended to overlap more songs. Subject males with UV-reduced neighbours gave a lower or similar response to neighbours compared to strangers. This indicates that male blue tits combine previously acquired information about an intruder’s plumage with familiarity of its song, and that their response depends on the perceived quality of the neighbour. This study provides evidence that familiarity in combination with multiple signals of quality may influence territorial relations among neighbours.     

What do we really know about the signalling role of plumage colour in blue tits? A case study of impediments to progress in evolutionary biology

Evolutionary biologists seek to explain the origin and maintenance of phenotypes, and a substantial portion of this research is accomplished by thorough study of individual species. For instance, many researchers study individual species to understand evolution of ornamental traits which appear to be products of sexual selection. I explored our understanding of sexual ornaments in a well‐studied vertebrate species that may serve as a case study for research programs in evolutionary biology. I attempted to located all published papers examining plumage colour and variables related to sexual selection hypotheses in a common European songbird, the blue tit (Cyanistes caeruleus). Researchers have estimated over 1200 statistical relationships with plumage colour of blue tits in 52 studies. However, of the approximately 1000 main‐effect relationships from the 48 studies that are candidates for inclusion in this meta‐analysis, more than 400 were reported without details of strength and direction. Circumstantial evidence suggests that an unknown number of other estimated effects remain unpublished. Missing information is a substantial barrier to interpretation of these papers and to meta‐analytic synthesis. Examination and analysis of funnel plots indicated that unpublished effects may be a biased sample of all effects, especially for comparisons of plumage colour to age and individual quality, and possibly also to measures of mate choice. Further, type I error was likely elevated by the large number of statistical comparisons evaluated, the frequent use of iterative model‐building procedures, and a willingness to interpret a wide variety of results as support for a hypothesis. Type I errors were made more problematic because blue tit plumage researchers only rarely have attempted to replicate important findings in their own work or that of others. Replication is essential to drawing robust scientific conclusions, especially in probabilistic systems with moderate to weak effects or a likelihood of bias. Last, researchers studying blue tit plumage have often developed ad hoc explanations for deviations of results from their predictions. Revising hypotheses in light of data is appropriate, but these revised hypotheses were rarely tested with new data. The only highly robust conclusion supported by meta‐analysis is that male blue tits have plumage that reflects more light in the ultraviolet and yellow wavelengths than the plumage of females. Various other effects, including condition‐dependence of plumage colour expression and a tendency for females to adjust the sex ratio of their offspring in response to male colour, remain uncertain. These obstacles to progress in the blue tit plumage literature are likely common in evolutionary biology, and so I recommend changes to incentive structures which may improve progress towards scientific understanding in this discipline.     

Carotenoid-based plumage colouration is associated with blood parasite richness and stress protein levels in blue tits (Cyanistes caeruleus)

Carotenoids are molecules that birds are not able to synthesize and therefore, must be acquired through their diet. These pigments, besides their function of giving birds red and yellow colouration when deposited in feathers, seem to act as immune-stimulators and antioxidants in the organism. Hence, only the healthiest individuals would be able to express carotenoid-based ornaments to a larger extent without compromising the physiological functions of carotenoids. Various studies have reported that birds infected by parasites are paler than those uninfected, but, to our knowledge, none of them has assessed the possible effect of multiple infections by blood parasites on plumage colour. By comparing the yellow colour in the breast plumage of blue tits, Cyanistes caeruleus, between birds infected by different numbers of blood parasite genera, we found that those birds infected by more than one genus were paler than those parasitized just by one. In addition, we examined the potential role of carotenoid-based plumage colour of blue tits as a long-term indicator of other parameters of health status, such as body condition and immunoglobulin and heat shock protein (HSP) levels. Our results indicate that more brightly coloured birds had lower HSP70 levels than paler birds, but we did not find any significant association between colour and body condition or immunoglobulin levels. In addition, we found a positive significant association between Haemoproteus density of infection and HSP60 levels. Overall, these results support the role of carotenoid-based colours as indicators of health status in blue tits and show detrimental effects of parasitism on this character.     

Age trajectories in extra-pair siring success suggest an effect of maturation or early-life experience

Across birds, male age is the most consistent predictor of extra-pair siring success, yet little is known about age effects on paternity over the lifetime of individuals. Here, we use data from a 13-year study of a population of blue tits (Cyanistes caeruleus) to investigate how extra-pair siring success changes with age within individuals. Our results indicate that extra-pair siring success does not continuously increase with male age. Instead, siring success was related to male age in a threshold fashion, whereby yearling males were less likely to gain paternity than older males. This effect was independent of the age of the social partner, but influenced by the age of the extra-pair female: success of yearlings at siring extra-pair young (EPY) with older females was even lower. Among males that sired at least one EPY, the number of extra-pair mates and the proportion of EPY sired were unrelated to male age. We found no evidence for an influence of selective disappearance on extra-pair reproduction. Senescence, if anything, only occurs at ages blue tits rarely reach. A literature review indicates that an effect of male age on extra-pair siring success may be limited to the switch from yearling to older in many species. Thus, the generally observed age effect on male extra-pair siring success may be linked to age class rather than continuous ageing. This suggests that lack of experience or not fully completed maturation are important drivers of age patterns in extra-pair paternity.     

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.     

Primary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits

The study of primary sex ratio adjustment in birds is notoriousfor inconsistency of results among studies. To develop our understandingof avian sex ratio variation, experiments that test a prioripredictions and the replication of previous studies are essential.We tested if female blue tits Parus caeruleus adjust the sexratio of their offspring to the sexual attractiveness of theirmates, as was suggested by a previous benchmark study on thesame species. In 2 years, we reduced the ultraviolet (UV) reflectanceof the crown feathers of males in the period before egg layingto decrease their attractiveness. In contrast to the simpleprediction from sex allocation theory, we found that the overallproportion of male offspring did not differ between broods ofUV-reduced and control-treated males. However, in 1 year, theUV treatment influenced offspring sex ratio depending on thenatural crown UV reflectance of males before the treatment.The last result confirms the pattern found in the previous bluetit study, which suggests that these complex patterns of primarysex ratio variation are repeatable in this bird species, warrantingfurther research into the adaptive value of blue tit sex ratioadjustment to male UV coloration.     

Female plumage coloration is sensitive to the cost of reproduction. An experiment in blue tits

1. A growing number of studies suggest that female ornaments are linked to maternal quality and influence male mate choice. These findings challenge the traditional male-biased view of sexual selection and the hypothesis that female ornaments are the outcome of a genetic correlation with male ornaments. To further test the hypothesis that female traits have a function, it is now essential to investigate their honesty and to determine how signalling and reproduction interact in females. If female traits are honest indicators of quality, then they are likely to have a specific signalling function. 2. We investigated whether carry-over effects of reproduction might ensure the honesty of plumage colour signalling of a bird species with conspicuous UV-blue and yellow coloration, the blue tit Cyanistes caeruleus. Reproductive effort was manipulated by removing clutches, thereby forcing both sexes to reproduce twice and to raise chicks later in the breeding season when food is less abundant. In the year following this manipulation, we investigated the change in plumage in experimental and control males and females. The change was measured in the two putative feather ornaments, the UV-blue cap and the yellow breast, and another feather trait probably less likely to be sexually selected: the wing length. We also tested whether higher-quality females had their coloration less affected by the experiment. 3. We found that control but not manipulated males and females increased their signal towards UV. In addition, in the manipulated group, females that were able to lay more eggs had their UV-blue coloration less affected by the treatment. For yellow coloration, we found that manipulated yearlings but not manipulated adults decreased their yellow chroma in comparison with control. Lastly, our results show that the condition of the manipulated females tended to be positively correlated with yellow chroma. 4. These results show that the trade-offs between reproduction and signalling can ensure the honesty of conspicuous plumage traits in female and male blue tits. In addition, they suggest that female traits have the potential to evolve under sexual selection in this and other bird species.     

Male colour variation in Spanish Pied Flycatchers Ficedula hypoleuca

Male variation in dorsal plumage colour was studied in a montane Spanish population of Pied Flycatchers Ficedula hypoleuca. Adult and yearling males did not differ in colour as measured by Drost's colour types. However, adult males differed from yearlings in being more likely to die if they were light-coloured the year before. Following the same individual males across years yielded a trend towards adult males becoming browner the following year, while no significant differences were found in first-year males. For surviving individual males, becoming browner between successive breeding seasons was associated with relative delays in breeding phenology. Significant but not very high repeatability of male colour is found, and this trait may be subjected to moderate environmental variation, perhaps while moulting in the winter quarters. Overall, being browner may be a sign of ageing and/or poor condition in Spanish Pied Flycatchers.     

Ultraviolet sexual dimorphism and assortative mating in blue tits

In spite of strong evidence for viability-based sexual selection and sex ratio adjustments, the blue tit, Parus caeruleus, is regarded as nearly sexually monomorphic and no epigamic signals have been found. The plumage coloration has not, however, been studied in relation to bird vision, which extends to the UV-A waveband (320 to 400 nm). Using molecular sex determination and UV/VIS spectrometry, we report here that blue tits are sexually dichromatic in UV/blue spectral purity (chroma) of the brilliant crown patch. It is displayed in courtship by horizontal posturing and erected nape feathers. A previously undescribed sexual dimorphism in crown size (controlling for body size) further supports its role as an epigamic ornament. Against grey-brown leaf litter and bark during pair formation in early spring, but also against green vegetation, UV contributes strongly to conspicuousness and sexual dimorphism. This should be further enhanced by the UV/bluish early morning skylight (''woodland shade'') in which blue tits display. Among 18 breeding pairs, there was strong assortative mating with respect to UV chroma, but not size, of the crown ornament. We conclude that blue tits are markedly sex dimorphic in their own visual world, and that UV/violet coloration probably plays a role in blue tit mate acquisition.