Carotenoid-based ornamentation and status signaling in the house finch

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

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.     

DELAYED PLUMAGE MATURATION IN PASSERINE BIRDS: RELIABLE SIGNALING BY SUBORDINATE MALES?

Three hypotheses (Cryptic, Female Mimicry, and Winter Adaptation) have been proposed to explain the occurrence of delayed plumage maturation (DPM) in passerine birds. We show that each of these hypotheses is really a composite of two different questions about: 1) the proximate function of dull plumage in second year (SY) males and 2) the selective mechanism that has favored that proximate function. We review the three hypotheses in the context of this distinction, and we find little evidence clearly supporting any of them. We propose a new Status Signaling Hypothesis (SSH) suggesting that dull SY male plumage is a reliable signal of subordinate. We suggest that female choice based on male plumage color (as an index of male quality) is the selective mechanism that has favored subordinate status signaling by SY males. If females prefer bright males, then dull plumage may be a reliable signal of subordinance and SY males may experience reduced levels of aggression from adult males. Male characters (like plumage color) are most likely to be the object of female choice when males defend simple nesting territories with little or no variation in territory quality. In such a system, SY males with low resource-holding potential would benefit (via matings or experience) by signaling subordinance and being allowed to settle among more brightly colored adults. Thus, DPM is expected to be more prevalent when males defend simple nesting territories. This prediction of the SSH is supported by data from the literature—a significantly higher proportion of species with DPM defend simple nesting territories (versus all-purpose territories) than do species without DPM.     

Status Signalling by Parus major: An Experiment in Deception

The ‘social control’ and ‘incongruence’ hypotheses, first put forward by ROHWER (1977) to explain how attempted ‘deceit’ status signalling is kept in check among winter-flocking birds, were tested under semi-natural conditions for Parus major. This species signals its social status by the width of its breast stripe. The lowest-ranked male in experimental flocks, each made up of four individuals, was manipulated in one of three ways: 1) the status signal was altered by painting the breast stripe to make it broader; 2) agonistic behaviour was altered by injecting testosterone; 3) both status signal and behaviour were manipulated. A study of the outcome of subsequent agonistic encounters by these birds revealed that the status of the manipulated individuals only rose when both their behaviour and status signal were altered. This indicates that the ‘social control’ hypothesis must be rejected, but not the ‘incongruence’ hypothesis.     

Extra-pair mate choice in the female great tit <Emphasis Type="Italic">Parus major</Emphasis>: good males or compatible males

The good genes hypothesis and the genetic compatibility hypothesis are the two main hypotheses that focus on the genetic benefit that a female can gain through her choice of a mate. We tested the two hypotheses on extra-pair mating in the great tit, Parus major. We found that female great tits choose males on the basis of breast stripe width, which is in accordance with the good genes hypothesis. Although females chose less related extra-pair males, the evidence for female choice for compatible males was overall weak. However, our data suggest a post-copulatory mechanism of inbreeding avoidance. The observed individual inbreeding coefficient, F, was similar for within-pair offspring (WPO) and extra-pair offspring (EPO). The observed individual F of WPO was lower than the expected individual F, whereas the observed F of EPO was similar to what was expected. These results highlight the importance of processes after copulation for the outcome of female mate choice. Our study shows that in a system with apparent pre-copulatory female choice for good genes, a post-copulatory mechanism may still promote the production of offspring that carry compatible genes.     

Plumage variability and territoriality in breeding turnstone Arenaria interpres: status signalling or individual recognition?

The turnstone Arenaria interpres has marked plumage variability in comparison with many other waders (shorebirds). Two hypotheses were tested in an attempt to explain plumage variability in breeding turnstones. The first, the status signalling hypothesis (SSH), suggests that plumage type signals status, and the second, the individual recognition hypothesis (IRH), suggests that plumage differences enable territorial birds to be recognized by their neighbours. The SSH was rejected by two tests: (a) there was no correlation between plumage phenotype of males and the quality of the territories they occupied; and (b) there was no correlation between the plumage phenotype of males and females paired to each other (assuming assortative mating according to rank). The IRH was supported by a test which showed that males could discriminate between neighbours and strangers on plumage differences alone: fibre-glass models mimicking neighbours were effectively ignored whilst models mimicking strangers elicited an aggressive response. It is stressed that this result does not demonstrate that plumage variability in breeding turnstones evolved to facilitate recognition by neighbours, and the potential of the IRH as an explanation of breeding plumage variability in waders is discussed.     

Plumage variability, status signalling and individual recognition in avian flocks

A decade ago it was suggested that much of the plumage variability exhibited by flocking birds can be explained by 'status signalling', plumage variability being used to signal agonistic status(1). As a result of this suggestion, a number of studies have examined the social significance of plumage differences, but the status signalling hypothesis has not received unequivocal support. Other factors, such as the facilitation of individual recognition, also appear to be important in explaining plumage variability.     

The relationship between social status and resting metabolic rate in great tits (Parus major) and pied flycatchers (Ficedula hypoleuca)

The oxygen consumption of great tits (Parus major) in winter flocks and of male pied flycatchers (Ficedula hypoleuca) in breeding condition, was measured. Resting metabolic rate was significantly correlated with dominance rank, as expressed by the width of the breast-stripe in the great tits and the darkness of the plumage on the head and back, or date of pair-formation, in males of the pied flycatcher. Individuals with the highest metabolic rates were the most dominant ones. Similarly, heart weight, relative to body weight, in dominant great tits was greater than that in lower-ranking birds.     

Stable correlation structure among multiple plumage colour traits: can they work as a single signal?

The presence of multiple distinct ornamental traits in the same species is frequently explained by context‐specificity and different information content. However, the expression of multiple ornaments is often correlated, and such traits may therefore function as a single, integrated signal. Delayed use of an integrated signal relative to production requires temporal stability in integration, which has seldom been examined. We used autumn and spring reflectance data from the breast, breast stripe, and crown of great tits (Parus major) to assess the stability and mating implications of colour signal integration, as well as the repeatability of any integrated colour trait and its correlation with condition during moult. We found high levels of stability between seasons, years, sexes, and ages in the correlation patterns of colour measures across the three plumage areas. The first principal component colour axis described joint variation of ultraviolet (UV) reflectance on the crown and the breast stripe, thereby representing an among‐trait UV chroma axis. However, only breast yellow chroma showed condition‐dependence, whereas temporally consistent and significant assortative mating was restricted to crown UV chroma. Our results therefore do not support the idea that the overall UV chroma of the breast stripe and the crown is special in condition‐dependence and repeatability, or that it plays a specific role in mutual sexual selection as an integrated signal. The results show that stable association between display traits is an existing phenomenon. They also indicate that, even in the presence of correlated traits, functional trait integration among these requires further scrutiny. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 92–108.     

Quantitative genetics of a carotenoid-based color: heritability and persistent natal environmental effects in the great tit

The information content of signals such as animal coloration depends on the extent to which variation reflects underlying biological processes. Although animal coloration has received considerable attention, little work has addressed the quantitative genetics of color variation in natural populations. We investigated the quantitative genetics of a carotenoid-based color patch, the ventral plumage of mature great tits (Parus major), in a wild population. Carotenoid-based colors are often suggested to reflect environmental variation in carotenoid availability, but numerous mechanisms could also lead to genetic variation in coloration. Analyses of individuals of known origin showed that, although plumage chromaticity (i.e., color) was moderately heritable, there was no significant heritability to achromaticity (i.e., brightness). We detected multiple long-lasting effects of natal environment, with hatching date and brood size both negatively related to plumage chromaticity at maturity. Our reflectance measures contrasted in their spatiotemporal sensitivity, with plumage chromaticity exhibiting significant spatial variation and achromatic variation exhibiting marked annual variation. Hence, color variation in this species reflects both genetic and environmental influences on different scales. Our analyses demonstrate the context dependence of components of color variation and suggest that color patches may convey multiple aspects of individual state.     

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

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

Structural coloration signals condition, parental investment, and circulating hormone levels in Eastern bluebirds (Sialia sialis)

Many of the brilliant plumage coloration displays of birds function as signals to conspecifics. One species in which the function of plumage ornaments has been assessed is the Eastern bluebird (Sialia sialis). Studies of a population breeding in Alabama (USA) have established that plumage ornaments signal quality, parental investment, and competitive ability in both sexes. Here we tested the additional hypotheses that (1) Eastern bluebird plumage ornamentation signals nest defense behavior in heterospecific competitive interactions and (2) individual variation in plumage ornamentation reflects underlying differences in circulating hormone levels. We also tested the potential for plumage ornaments to signal individual quality and parental investment in a population breeding in Oklahoma (USA). We found that Eastern bluebirds with more ornamented plumage are in better condition, initiate breeding earlier in the season, produce larger clutches, have higher circulating levels of the stress hormone corticosterone, and more ornamented males have lower circulating androgen levels. Plumage coloration was not related to nest defense behavior. Thus, plumage ornamentation may be used by both sexes to assess the physiological condition and parental investment of prospective mates. Experimental manipulations of circulating hormone levels during molt are needed to define the role of hormones in plumage ornamentation.     

Measurement of plumage badges: an evaluation of methods used in the Great Tit Parus major

There is an increasing interest in the variation in plumage coloration and a number of theories have been proposed to explain its evolution (Butcher & Rohwer 1989, Savalli 1995). Birds haye been considered to signal through plumage their dominance status, ability to evade predators, parasite resistance or for example their parental care abilities (reviewed in Butcher & Rohwer 1989, Anderson 1994, Savalli 1995, Johnstone 1997). However, the measuremcnt of plumage badges and its accuracy have received little attention (Savalli 1995). In the case of the Great Tit Parus major, for instance, several studies have analysed the importance of the breast stripe size as an indicator of dominance status in winter flocks (Jarvi & Bakken 1984, Piiysa 1988, Lemel 1989, Wilson 1992) and its importance in mate choice (Norris 1990, 1993), but the badgc has been estimated using very different indices, even in studies performed by the same authors (Norris 1990, 1993). We compare the performance of differvnt indices in estimating Great Tit stripe size, by comparing them with badge surface area obtained from image analysis of digital photographs. We propose that digital photography provides a reliable and inexpensive method to measure plumage badges in birds and we demonstrate its performance in the Great Tit.     

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.     

Ontogenetic variation in the plumage colour of female European Pied Flycatchers Ficedula hypoleuca

Although variation in the dorsal plumage colour of male European Pied Flycatchers Ficedula hypoleuca has received a great deal of attention, females of the species have been usually considered to be nearly uniformly monochromatic brown. Using reflectance spectrophotometry, we explore the age‐dependent variation of plumage colour in females. We disentangle the within‐ and between‐individual effects of this pattern and show a within‐individual darkening of the mantle colour with age, whereas differences between individuals in structural colour expression may underlie the trend for a more reflective white in the females' breast plumage with advancing age. The darkening of the dorsal plumage as females age reflects the most common pattern of age‐related variation in males in most European populations of the species.     

Ultraviolet reflectance of plumage for parent-offspring communication in the great tit (Parus major)

Ultraviolet (UV) reflectance has been implicated in mate selection.Yet, in some bird species the plumage of young varies in UVreflectance already in the nest and long before mate choiceand sexual selection come into play. Most birds molt the juvenilebody plumage before reaching sexual maturity, and thus, someconspicuous traits of the juvenile body plumage may rather haveevolved by natural selection, possibly via predation or parentalpreference. This second hypothesis is largely untested and predictsa differential allocation of food between fledging and totalindependence, which is a time period of 2–3 weeks whereoffspring mortality is also highest. Here, we test the predictionthat parents use the individual variation in UV reflectanceamong fledglings for differential food allocation. We manipulatedUV reflectance of the plumage of fledgling great tits Parusmajor by treating chest and cheek feathers with a lotion thateither did or did not contain UV blockers and then recordedfood allocation by parents in an outdoor design simulating postfledgingconditions. The visible spectrum was minimally affected by thistreatment. Females were found to feed UV-reflecting offspringpreferentially, whereas males had no preference. It is the firstevidence showing that the UV reflectance of the feathers ofyoung birds has a signaling function in parent–offspringcommunication and suggests that the UV traits evolved via parentalpreference.     

Changes in the flocking behaviour of wintering English titmice with time,weather and supplementary food

Over the course of one winter, the food supply of birds living in a deciduous woodland in southern England was supplemented and unsupplemented during alternating periods. In the presence of substantial predation pressure from hawks, the sociality of blue tits, Parus caeruleus, and great tits, P. major, showed significant partial correlations with several weather and temporal factors when the woodland was unsupplemented. Such correlations between social behaviour and abiotic factors diminished significantly when the birds had access to extra food. Blue tits and great tits without access to supplemental food flocked significantly more often with other species while foraging than when they were food-supplemented. Long-tailed tits, Aegithalos caudatus, ignored the artificial food and foraged in mixed-species flocks to the same extent in both unsupplemented and food-supplemented periods. Results disprove the hypothesis that mixed-species foraging groups are caused by increased predation protection alone, and they support the hypotheses that mixed-species foraging groups are caused by increased foraging efficiency alone or by a combination of increased foraging efficiency and increased protection from predators.     

Sources of distinctness of juvenile plumage in Western Palearctic passerines

Juveniles of many avian species possess a spotted or mottled body plumage that is visually distinct from the plumage of adults. In other species, however, juveniles fledge with a body plumage that is just a pale representation of adult female plumage. The reasons for this variation are poorly understood. Several hypotheses concerning social (parent–offspring, adult–juvenile, juvenile–juvenile), ecological (predation risk) and physiological (costs of plumage development) implications of juvenile body plumage are presented in relation to predictions concerning associations with certain ecological and life‐history attributes of avian species. In the present study, we conduct a phylogenetically corrected comparative analysis of Western Palearctic passerines looking for sources of variation in the incidence of distinct and adult‐like juvenile body plumages. We scored plumages based on plates in the Handbook of the Birds of the Western Palearctic (Cramp & Perrins, 1988–1994; Oxford University Press) (HBWP) and entered body mass, migratory habits, habitat, nestling diet, breeding dispersion, gregariousness, duration of the nestling period, type of nest, conspicuousness of female plumage, and sexual dimorphism as explanatory variables, as presented in HBWP, in phylogenetic generalized least square regression analyses. One‐third of the species presented distinct juvenile body plumages, which lasted on average for the first 2 months of life. Body mass, conspicuousness of female plumage, migratory habits, and habitat were significantly associated with interspecific variation in distinctness of juvenile plumage, with smaller species, more conspicuous species, migrants, and species from forested habitats showing distinct juvenile plumages with higher frequency. The phylogenetic signal was moderately high. Assuming that conspicuous adult plumage is costlier to produce than distinct juvenile body plumage (pigments, conspicuousness), the need to acquire social status among juveniles before the winter may explain the more adult‐like plumage in resident species because juveniles will probably compete with individuals that they may have known during their first months of life. On the other hand, migrant juveniles may compete with a different set of individuals in winter quarters and can use savings in resources necessary for developing adult‐like plumages to improve migration capacity by allocating resources to other functions. The association with habitat could be related to juveniles in open habitats participating in more extended interactions with other juveniles than in forested habitats where lower visibility may reduce the capacity to detect or respond to signals from juvenile conspecifics. More studies on this possibly crucial life stage are needed. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 440–454.     

Early learning affects social dominance: interspecifically cross-fostered tits become subdominant

Social dominance influences the outcome of competitive interactionsover limited resources, and may hence be important for individualfitness. Theory thus predicts that its heritability will below and that non-genetic determinants of dominance should prevail.In this field experiment we reciprocally cross-fostered greattits (Parus major) to blue tits (Parus caeruleus) to investigatethe impact of early social experience on dominance status incompetition over food during winter. Controlling for potentialeffects of age, size, sex and site-related dominance, we showthat cross-fostered birds of both species were subdominant toconspecific immigrants, while controls originating from unmanipulatedbroods were dominant to conspecific immigrants. Furthermore,blue tits reared by blue tit parents but with at least one greattit broodmate had lower dominance status relative to conspecificimmigrants than did controls. Although great tits generallydominated blue tits, cross-fostered birds of both species initiatedmarginally more fights against the other species than did theirrespective controls, suggesting faulty species recognition.Since both social parents and broodmates strongly influencethe dominance behavior of offspring later in life, we concludethat social conditions experienced at an early age are crucialfor the determination of subsequent social dominance.     

Offspring sex ratio is related to male body size in the great tit (Parus major)

Sex allocation theory predicts that the allocation of resourcesto male and female function should depend on potential fitnessgain realized through investment in either sex. In the greattit (Parus major), a monogamous passerine bird, male resourceholdingpotential (RHP) and fertilization success both depend on malebody size (e.g., tarsus length) and plumage traits (e.g., breaststripe size). It is predicted that the proportion of sons ina brood should increase both with male body size and plumage traits,assuming that these traits show a father—offspring correlation. Thiswas confirmed in our study: the proportion of sons in the brood increasedsignificantly with male tarsus length and also, though not significantly,with the size of the breast stripe. A sex ratio bias in relationto male tarsus length was already present in the eggs because(1) the bias was similar among broods with and without mortalitybefore the nestlings' sex was determined, and (2) the bias remainedsignificant when the proportion of sons in the clutch was conservativelyestimated, assuming that differential mortality before sex determinationcaused the bias. The bias was still present among recruits.The assumption of a father—offspring correlation was confirmedfor tarsus length. Given that both RHP and fertilization successof male great tits depend on body size, and size of father andoffspring is correlated, the sex ratio bias may be adaptive.