The effect of dietary carotenoid access on sexual dichromatism and plumage pigment composition in the American goldfinch

We investigated potential dietary and biochemical bases for carotenoid-based sexual dichromatism in American goldfinches (Carduelis tristis). Captive male and female finches were given access to the same type and amount of carotenoid pigments in the diet during their nuptial molt to assess differences in the degree to which the two sexes incorporated ingested pigments into their plumage. When birds were fed a uniform, plain-seed diet, or one that was supplemented with the red carotenoid canthaxanthin, we found that males grew more colorful plumage than females. HPLC analyses of feather pigments revealed that male finches incorporated a higher concentration of carotenoids into their pigmented feathers than females. Compared to females, males also deposited significantly more canary xanthophyll B into feathers when fed a plain-seed diet and a greater concentration and proportion of canthaxanthin when fed a carotenoid-supplemented diet. These results indicate that sex-specific expression of carotenoid pigmentation in American goldfinches may be affected by the means by which males and females physiologically utilize (e.g. absorb, transport, metabolize, deposit) carotenoid pigments available to them in the diet.     

Lutein-based plumage coloration in songbirds is a consequence of selective pigment incorporation into feathers

Many birds obtain colorful carotenoid pigments from the diet and deposit them into growing tissues to develop extravagant red, orange or yellow sexual ornaments. In these instances, it is often unclear whether all dietary pigments are used as integumentary colorants or whether certain carotenoids are preferentially excluded or incorporated into tissues. We examined the carotenoid profiles of three New World passerines that display yellow plumage coloration—the yellow warbler (Dendroica petechia), common yellowthroat (Geothlypis trichas) and evening grosbeak (Coccothraustes vespertinus). Using high-performance liquid chromatography, we found that all species used only one carotenoid—lutein—to color their plumage yellow. Analyses of blood carotenoids (which document those pigments taken up from the diet) in two of the species, however, revealed the presence of two dietary xanthophylls—lutein and zeaxanthin—that commonly co-occur in plants and animals. These findings demonstrate post-absorptive selectivity of carotenoid deposition in bird feathers. To learn more about the site of pigment discrimination, we also analyzed the carotenoid composition of lipid fractions from the follicles of immature yellow-pigmented feathers in G. trichas and D. petechia and again detected both lutein and zeaxanthin. This suggests that selective lutein incorporation in feathers is under local control at the maturing feather follicle.     

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

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

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.     

基于类胡萝卜素着色的鸟类羽色多样性形成机制

人们对动物体色的研究由来已久。作为一类让生物呈现出多变色彩的重要色素, 类胡萝卜素可以在鸟类的羽毛、鸟喙和皮肤等体表组织中沉积, 产生红、橙、黄、粉、紫等颜色。类胡萝卜素不能在鸟类体内合成, 需从食物中摄取, 进而在体内完成吸收、运输、代谢和沉积等一系列过程, 才能用于羽毛着色。与类胡萝卜素着色相关的生理及遗传调控机制一直备受关注, BCO2、SCARB1和CYP2J19等影响类胡萝卜素在鸟类羽毛中着色的关键基因, 推动了对羽色遗传调控机制的深入认识。本文介绍了鸟类可利用类胡萝卜素的主要类型和基本特征, 综述了类胡萝卜素着色相关的生理过程以及调控基因研究的最新进展, 旨在增加对鸟类羽毛中类胡萝卜素着色过程和相关遗传机制的理解。     

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

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

The kinds of traits involved in male--male competition: a comparison of plumage, behavior, and body size in quail

I compared the role of ornate plumage, behavior, and body sizeduring male—male competition in two species of New Worldquail. Gambel's quail (Callipepla gambelii) is a highly ornateand dichromatic species, whereas scaled quail (C. squamata)is unornamented and monochromatic. During paired contests betweenunfamiliar males, high rates of testosterone-mediated behaviors(tidbitting, calling) and large body size (mass, tarsus, andtail length) corresponded to winners. In the highly ornate Gambel's quail, male head plumes also influenced the outcomeof contests. Plume enhancement made Gambel's quail more likelyto win contests, whereas plume removal made males more likelyto lose. Plume position also reflected male status. Winningmales erected plumes, whereas losers frequently flattened them.Some plumage ornaments, such as belly patches, did not playa primary role during male contests. Unlike static ornaments,head plumes are highly modifiable and likely signal immediateinformation regarding a male's intent, similar to a coverablebadge. Combined, intrasexual selection favored dynamic traits(fast display rates, modifiable ornaments) and static traits(body size) as indicators of male condition or motivation.In scaled quail only, male size was favored both by male—malecompetition and female choice. Accordingly, the degree of sizedimorphism (tarsus length) is greater in scaled than in Gambel'squail. The frequency of overt aggression (chases, pecks, displacement)also differed between species. Gambel's quail were very aggressive,and subordinates often challenged their opponents. In contrast, scaled quail were less aggressive, and subordinates rarely disputedrank. Interspecific comparison indicated differences in themaintenance of male status and possibly in the honesty of signaling.Both appear to be related to differences in social system.     

The role of Drosophila ninaG oxidoreductase in visual pigment chromophore biogenesis

We previously reported (Sarfare, S., Ahmad, S. T., Joyce, M. V., Boggess, B., and O'Tousa, J. E. (2005) J. Biol. Chem. 280, 11895-11901) that the Drosophila ninaG gene encodes an oxidoreductase involved in the biosynthesis of the (3S)-3-hydroxyretinal serving as chromophore for Rh1 rhodopsin and that ninaG mutant flies expressing Rh4 as the major opsin accumulate large amounts of a different retinoid. Here, we show that this unknown retinoid is 11-cis-3-hydroxyretinol. Reversed phase high performance liquid chromatography coupled with a photodiode array UV-visible absorbance detector and mass spectrometer revealed a major product eluting at a retention time, t(r), of 3.5 min with a lambda(max) of approximately 324 nm and with a base peak in the mass spectrum at m/z 285. These observations are identical with those of the 3-hydroxyretinol standard. The base peak in the electrospray ionization mass spectrum arises from the loss of a water molecule from the protonated molecule at m/z 303 because of fragmentation in the ion source. These results suggest that 11-cis-3-hydroxyretinol is an intermediate required for chromophore biogenesis in Drosophila. We further show that ninaG mutants fed on retinal as the sole source of vitamin A are able to synthesize 3-hydroxyretinoids. Thus, the NinaG oxidoreductase is not responsible for the initial hydroxylation of the retinal ring but rather acts in a subsequent step in chromophore production. These data are used to review chromophore biosynthesis and propose that NinaG acts in the conversion of (3R)-3-hydroxyretinol to the 3S enantiomer.     

The role of a long-wavelength pigment form in the chlorophyll biosynthesis

Photoconversion of protochlorophyllide₆₅₀ form was observed in etiolated leaves illuminated with long-wavelength—690 nm—light. This process showed Shibata shift and was found to have a strong temperature dependence between 20 and –40°C. The low rate of reaction, the strong temperature dependence and calculations on the spectral overlap integral of absorption and fluorescence bands in this spectral region indicate that the phototransformation of the 650 nm form of protochlorophyllide may be caused by a back energy migration from a long-wavelength pigment form absorbing around 690 nm; this pigment form is probably a long-wavelength form of protochlorophyll/ide.     

The role of life history traits in mammalian invasion success

Why some organisms become invasive when introduced into novel regions while others fail to even establish is a fundamental question in ecology. Barriers to success are expected to filter species at each stage along the invasion pathway. No study to date, however, has investigated how species traits associate with success from introduction to spread at a large spatial scale in any group. Using the largest data set of mammalian introductions at the global scale and recently developed phylogenetic comparative methods, we show that human‐mediated introductions considerably bias which species have the opportunity to become invasive, as highly productive mammals with longer reproductive lifespans are far more likely to be introduced. Subsequently, greater reproductive output and higher introduction effort are associated with success at both the establishment and spread stages. High productivity thus supports population growth and invasion success, with barriers at each invasion stage filtering species with progressively greater fecundity.     

SWS2 visual pigment evolution as a test of historically contingent patterns of plumage color evolution in warblers

Distantly related clades that occupy similar environments may differ due to the lasting imprint of their ancestors—historical contingency. The New World warblers (Parulidae) and Old World warblers (Phylloscopidae) are ecologically similar clades that differ strikingly in plumage coloration. We studied genetic and functional evolution of the short‐wavelength‐sensitive visual pigments (SWS2 and SWS1) to ask if altered color perception could contribute to the plumage color differences between clades. We show SWS2 is short‐wavelength shifted in birds that occupy open environments, such as finches, compared to those in closed environments, including warblers. Phylogenetic reconstructions indicate New World warblers were derived from a finch‐like form that colonized from the Old World 15–20 Ma. During this process, the SWS2 gene accumulated six substitutions in branches leading to New World warblers, inviting the hypothesis that passage through a finch‐like ancestor resulted in SWS2 evolution. In fact, we show spectral tuning remained similar across warblers as well as the finch ancestor. Results reject the hypothesis of historical contingency based on opsin spectral tuning, but point to evolution of other aspects of visual pigment function. Using the approach outlined here, historical contingency becomes a generally testable theory in systems where genotype and phenotype can be connected.     

Carotenoid‐based plumage coloration in golden‐crowned kinglets Regulus satrapa: pigment characterization and relationships with migratory timing and condition

Carotenoid‐based ornamental coloration has long been proposed to honestly signal quality due to its dependence on individual condition. Because migration can be one of the most stressful periods of an animal's annual cycle, developing colourful plumage may be particularly challenging for species in which migration and moult periods overlap or occur sequentially. The purpose of this study was to investigate pigmentary and condition‐dependent bases of carotenoid colour variation in a small migratory passerine, the golden‐crowned kinglet Regulus satrapa (Family Regulidae). We captured 186 male and female kinglets of various ages during fall migration in southwestern Ontario, Canada and recorded arrival date, body condition index, fat and pectoral muscle scores, wing mite infestation, and feather growth rate as measures of condition. We quantified crown coloration using reflectance spectrometry and analyzed feather carotenoids using high‐performance liquid chromatography. Yellow crown feathers of female kinglets contained only yellow hydroxycarotenoids, whereas orange feathers of males harboured a suite of eight carotenoid pigments. Males with longer wavelength orange crown hues deposited greater concentrations of ketocarotenoids, especially canthaxanthin. Female kinglets with longer wavelength crown hues and males with longer wavelength crown hues and more saturated crown coloration left for migration earlier in the year. Females with longer wavelength crown hues had fewer feather mites and tended to be in better condition. However, male kinglets with more saturated coloration possessed smaller pectoral muscles. This is the first study to identify plumage carotenoids in this North American bird family and to determine the pigmentary basis for both inter‐ and intrasexual colour variation. Our results provide further support for the condition‐dependence of carotenoid coloration and suggest that ornamental elaboration in both sexes may encode information about fall condition and migratory performance.     

The role of reflecting pigment cells in the turnover of crayfish photoreceptors

Summary The photoreceptors of the crayfish Procambarus clarkii undergo an extensive cycle of turnover in the late afternoon. Quantitative light and electron microscopy reveal a sharp increase in the fractional volume (i.e., density) of reflecting-pigment-cell granules and vacuoles shortly following late-afternoon photoreceptor turnover. The reflecting pigment cells (RPCs), which permanently reside within the crayfish retina, are shown to serve much the same function as the vertebrate pigment epithelium. The RPCs phagocytose partially digested photoreceptive microvilli and the ingested debris is degraded further into the granules and vacuoles which characterize these cells. Phagosome degradation appears to be mediated by Golgi complexes. Acid phosphatase appears to be involved in the initial rhabdom breakdown but not in the final reduction of RPC granules.     

Testosterone levels in relation to size and UV reflectance of achromatic plumage traits of female pied flycatchers

In a substantial number of species, females show some development of secondary sexual characters. These traits can function as signals of individual phenotypic or genetic qualities and status to conspecifics. Individuals may benefit potentially from expressing signals or badges of status if they are reliable and honest signals of individual quality. In many species, badge sizes have been shown to correlate with dominance rank, which may be mediated by testosterone (T) levels. Here, we explored geographic variation in the size and properties of the white wing patch of female pied flycatchers Ficedula hypoleuca and its relation to circulating T levels in three populations (two southern populations in central Spain and a northern population in Finland). Furthermore, we aimed at detecting if the size of the white wing patch and its ultraviolet (UV) reflectance indicate individual quality. We found that females in Spain had larger, brighter and more UV reflecting wing patches than those in Finland. Females with higher UV reflectance and larger primary white patches bred earlier. Younger females and females with larger primary white wing patches showed higher T levels. In contrast, higher values of UV reflectance in feathers from these patches were associated with low T levels. Despite genetic differentiation and differences in trait expression between populations, female pied flycatchers from different populations may converge and use the size of white wing patches to signal their T levels and thereby their social dominance.     

The ubiquity of avian ultraviolet plumage reflectance

Although several bird species have been shown to reflect ultraviolet (UV) light from their plumages, the incidence of UV reflectance, and therefore the potential for UV or UV-enhanced signals, across the avian tree of life is not known. In this study, we collected reflectance data from the plumages of 312 bird species representing 142 families. Our results demonstrate that all avian families possess plumages that reflect significant amounts of UV light. The ubiquity of UV reflectance indicates that all studies of avian behaviour, ecology and evolution involving plumage coloration would benefit from consideration of plumage reflectance in the UV portion of the electromagnetic spectrum. Additionally, we demonstrate the existence of cryptic UV plumage patches and cryptic dimorphism among birds.     

Condition-dependent variation in the blue-ultraviolet coloration of a structurally based plumage ornament

After years of investigation into the function of sexually dimorphic ornamental traits, researchers are beginning to understand how bright plumage colour in birds acts as an intraspecific signal. This work has focused primarily on pigment-based ornaments because they are highly variable in patch size, hue and brightness for some species. In contrast, structurally based ornaments have been little studied, in part because they do not appear to be as variable as pigment-based ornaments. We investigated a structurally based plumage ornament in a wild population of blue grosbeaks (Guiraca caerulea), a sexually dimorphic passerine. We report plumage variation that extends into the ultraviolet region of the spectrum. The pattern of covariation between four out of five elements of plumage variation suggests that structurally based ornamentation is pushed towards extreme expression of the trait as predicted by the sexual selection theory. The ''bluest'' birds have the highest percentage of blue feathers on the body. These ornamental feathers reflect light maximally at the shortest wavelengths (ultraviolet), with the greatest intensity and the greatest contrast. Age may have some effect on expression of blueness. In addition, plumage variables are correlated with growth bars in tail feathers (a record of nutritional condition during moult in a non-ornamental trait). This suggests that the ornament is partially condition dependent. Thus, blue plumage in male grosbeaks may serve as an honest indicator of age and quality.