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Mechanics of Carotenoid-Based Coloration

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... These pigments must be ingested with the food as most animals cannot de novo synthesise them (e.g. McGraw, 2006;Maoka, 2021). These compounds also have relevant functions in homeostasis as antioxidants and immune boosters (e.g. ...
... Red 4C-ketocarotenoids in coloured traits are enzymatically synthesized from dietary yellow carotenoids in many animal species (McGraw, 2006;Twyman et al., 2016). It has been suggested that the enzymes in charge of 4C-ketocarotenoid synthesis are located in the inner mitochondrial membrane ("IMM"; Johnson and Hill, 2013;Cantarero and Alonso-Alvarez, 2017;Hill et al., 2019). ...
... Prum et al., 2012;Friedman et al., 2014;Badyaev et al., 2017;Hudon et al., 2021). The carotenoid-transformation enzymes may catalyze oxidation (oxidases), hydroxylation (hydroxylases) or dehydrogenation (dehydrogenases) on substrate carotenoids, but red 4C-ketocarotenoids specifically require adding a ketone group via oxidation (McGraw, 2006). This ketone addition elongates the molecule's conjugated system, raising the carotenoid's peak absorbance wavelength and making the trait redder (Britton, 2008). ...
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In many vertebrates, dietary yellow carotenoids are enzymatically transformed into 4C-ketocarotenoid pigments, leading to conspicuous red colourations. These colourations may evolve as signals of individual quality under sexual selection. To evolve as signals, they must transmit reliable information benefiting both the receiver and the signaler. Some argue that the reliability of 4C-ketocarotenoid-based colourations is ensured by the tight link between individual quality and mitochondrial metabolism, which is supposedly involved in transforming yellow carotenoids. We studied how a range of carotenoids covary in the feathers and blood plasma of a large number (n > 140) of wild male common crossbills (Loxia curvirostra). Plumage redness was mainly due to 3-hydroxy-echinenone (3HOE). Two other, less abundant, red 4C-ketocarotenoids (astaxanthin and canthaxanthin) could have contributed to feather colour as they are redder pigments. This was demonstrated for astaxanthin but not canthaxanthin, whose feather levels were clearly uncorrelated to colouration. Moreover, moulting crossbills carried more 3HOE and astaxanthin in blood than non-moulting ones, whereas canthaxanthin did not differ. Canthaxanthin and 3HOE can be formed from echinenone, a probable product of dietary β-carotene ketolation. Echinenone could thus be ketolated or hydroxylated to produce canthaxanthin or 3HOE, respectively. In moulting birds, 3HOE blood levels positively correlated to astaxanthin, its product, but negatively to canthaxanthin levels. Redder crossbills also had lower plasma canthaxanthin values. A decrease in hydroxylation relative to ketolation could explain canthaxanthin production. We hypothesize that red colouration could indicate birds' ability to avoid inefficient deviations within the complex enzymatic pathways.
... These 44 pigments must be ingested with the food as most animals cannot de novo synthesise them 45 (e.g. McGraw, 2006;Maoka, 2021). These compounds also have relevant functions in 46 homeostasis as antioxidants and immune boosters (e.g. ...
... Evolutionary theory states that signal reliability 52 can be maintained by production/maintenance costs, which should be disproportionally 53 high for low-quality individuals who reduce signal expression (e.g. Grafen, 1990 on Stradi (1998) and Mcgraw (2006 terms in the statistical analyses (see below). They were sexed, aged and ringed as described ...
... ). The carotenoid-transformation enzymes may induce oxidation (oxidases), hydroxylation (hydroxylases) or dehydrogenation (dehydrogenases) on substrate78 carotenoids, but red 4C-ketocarotenoids specifically require adding a ketone group via 79 oxidation (ketolases;McGraw, 2006). This ketone addition elongates the molecule's 80 conjugated system, raising the carotenoid's peak absorbance wavelength and making the This preprint research paper has not been peer reviewed. ...
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ABSTRACT: In many vertebrates, dietary yellow carotenoids are enzymatically transformed into 4C-ketocarotenoid pigments, leading to conspicuous red colourations. These colourations may evolve as signals of individual quality under sexual or social selection. To evolve as signals, they must transmit reliable information benefiting both the receiver and the signaler. Some argue that the reliability of 4C-ketocarotenoid-based colourations is ensured by the tight link between individual quality and cell (mitochondrial) metabolism, which is supposedly involved in transforming yellow carotenoids. We studied how a range of carotenoids covary in the feathers and blood plasma of a large number (n > 140) of wild male common crossbills (Loxia curvirostra). Plumage redness was mainly due to 3-hydroxy-echinenone (3HOE). Two other red 4C-ketocarotenoids, although less abundant (astaxanthin and canthaxanthin), could have contributed to feather colour as they are redder pigments. This was demonstrated for astaxanthin but not canthaxanthin, whose feather levels were uncorrelated to colouration. Moreover, moulting crossbills carried more 3HOE and astaxanthin in blood than non-moulting ones, but canthaxanthin did not differ. Canthaxanthin and 3HOE are formed from echinenone, a product of dietary β-carotene ketolation. Echinenone is ketolated or hydroxylated to produce canthaxanthin or 3HOE, respectively. In moulting birds, astaxanthin blood levels positively correlated to 3HOE, its precursor, but negatively to canthaxanthin levels. Redder birds also had lower plasma canthaxanthin values. An imbalance in the activity (or level) of ketolases (e.g. CYP2J19) and hydroxylases (unknown) may explain canthaxanthin production. We hypothesise that red colouration could indicate birds’ ability to avoid inefficiencies in complex enzymatic pathways.
... Pigmentary coloration is widely distributed in animals and serves many functions including camouflage, interspecific signaling (e.g., warning coloration), and intraspecific signaling (e.g., mate attraction; reviewed in Andersson 1994;Espmark et al. 2000;Hill and McGraw 2006). Pigmentary coloration is often subdivided by predominant pigments, such as carotenoid-based coloration, eumelanin-based coloration, and pheomelanin-based coloration (e.g., see McGraw 2006aMcGraw , 2006b on bird coloration). It is then not surprising that the evolutionary and ecological features of animal coloration are often attributed to the chemical properties of predominant pigments. ...
... The function of feather porphyrin has not been known (reviewed in McGraw 2006c), but it might function as an "ephemeral" signal because porphyrin is easily photodegraded (Galván et al. 2016). By depositing porphyrin rather than more stable alternatives, such as pheomelanin pigments, which also provide a rusty or brown appearance (McGraw 2006b(McGraw , 2006c, birds might display conspicuous coloration for only a short period and may even directly signal the freshness of the feathers (Galván et al. 2016). However, the effect of porphyrin on feather color change, particularly in its importance relative to the predominant feather pigments (e.g., pheomelanin), remains to be clarified. ...
... The observed porphyrin content is low even when compared with other species, such as the barn owl Tyto alba, in which protoporphyrin IX content was one-tenth of pheomelanin pigments . Previous studies often focused on the predominant pigments such as carotenoids and melanins, assuming that the evolutionary and ecological features of integument coloration can be attributed to the chemical properties of these predominant pigments (e.g., see McGraw 2006b, Roulin 2016 for reviews on melanin-based feather coloration). However, as was shown here, feather color change, an ecological feature of feather coloration, depends on a minority pigment, and thus, the assumption that predominant pigments determine the evolutionary and ecological features of animal coloration is no longer valid. ...
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Pigmentary coloration is widespread in animals. Its evolutionary and ecological features are often attributed to the property of predominant pigments; therefore, most research has focused on predominant pigments such as carotenoids in carotenoid-based coloration. However, coloration results from predominant pigments and many other minority pigments, and the importance of the latter is overlooked. Here, we focused on porphyrin, an “uncommon” pigment found in bird feathers, and investigated its importance in the context of feather color changes in the barn swallow Hirundo rustica. We found that the “pheomelanin-based coloration” of the barn swallow faded after the irradiation of UV light, and this effect was particularly strong in the feathers of young swallows (nestlings and fledglings, here). We also found that it is not the predominant pigment, pheomelanin, but protoporphyrin IX pigment that showed the same pattern of depigmentation after the irradiation of UV light, particularly in the feathers of young swallows. In fact, the abovementioned age-dependent feather color change was statistically explained by the amount of porphyrin in the feathers. The current study demonstrates that a minority pigment, porphyrin, explains within-season dynamic color change, an ecological feature of feather coloration. The porphyrin-mediated rapid color change would benefit young birds, in which feather coloration affects the parental food allocation during a few weeks before independence, but not later. Future studies should not ignore these minor but essential pigments and their evolutionary and ecological functions.
... Carotenoids are the primary source of red and yellow coloration birds (Mcgraw, 2006), turtles (Steffen et al., 2015) and crustaceans (Weaver, Cobine & Hill, 2018a) and play important roles in yellow and red coloration in fish (Luo et al., 2021) and reptiles (Olsson, Stuart-Fox & Ballen, 2013). In vertebrates and, with very few exceptions (Altincicek, Kovacs & Gerardo, 2012), in invertebrates, carotenoids cannot be synthesised de novo from basic precursor molecules; they must be ingested (Goodwin, 1984;Weaver et al., 2018a). ...
... In vertebrates and, with very few exceptions (Altincicek, Kovacs & Gerardo, 2012), in invertebrates, carotenoids cannot be synthesised de novo from basic precursor molecules; they must be ingested (Goodwin, 1984;Weaver et al., 2018a). Carotenoids are used as ornamental colorants through one of three biochemically distinct processes: (i) ingested, dietary pigments are used without biochemical modification; (ii) dietary pigments are biochemically modified into ε,ε-carotenoids via a dehydrogenase reaction; or (iii) dietary pigments are biochemically modified into keto-carotenoids via a ketolation reaction using the products of a dehydrogenation reaction as precursors, which often involves a pigmentary colour change, usually yellow to red (Mcgraw, 2006;Hill & Johnson, 2012;Toomey et al., 2022) (Fig. 2). Decades of work on the pigmentary basis for yellow and red coloration in birds has revealed that all three means of displaying carotenoid coloration are common in Aves (Mcgraw, 2006;Friedman, McGraw & Omland, 2014;Ligon et al., 2016) as well as in closely related but extinct taxa (Davis & Clarke, 2022) and that all three sources of coloration are used at least occasionally in diverse taxa of vertebrates and invertebrates (Goodwin, 1984). ...
... Carotenoids are used as ornamental colorants through one of three biochemically distinct processes: (i) ingested, dietary pigments are used without biochemical modification; (ii) dietary pigments are biochemically modified into ε,ε-carotenoids via a dehydrogenase reaction; or (iii) dietary pigments are biochemically modified into keto-carotenoids via a ketolation reaction using the products of a dehydrogenation reaction as precursors, which often involves a pigmentary colour change, usually yellow to red (Mcgraw, 2006;Hill & Johnson, 2012;Toomey et al., 2022) (Fig. 2). Decades of work on the pigmentary basis for yellow and red coloration in birds has revealed that all three means of displaying carotenoid coloration are common in Aves (Mcgraw, 2006;Friedman, McGraw & Omland, 2014;Ligon et al., 2016) as well as in closely related but extinct taxa (Davis & Clarke, 2022) and that all three sources of coloration are used at least occasionally in diverse taxa of vertebrates and invertebrates (Goodwin, 1984). ...
Article
Even as numerous studies have documented that the red and yellow coloration resulting from the deposition of carotenoids serves as an honest signal of condition, the evolution of condition dependency is contentious. The resource trade-off hypothesis proposes that condition-dependent honest signalling relies on a trade-off of resources between ornamental display and body maintenance. By this model, condition dependency can evolve through selection for a re-allocation of resources to promote ornament expression. By contrast, the index hypothesis proposes that selection focuses mate choice on carotenoid coloration that is inherently condition dependent because production of such coloration is inexorably tied to vital cellular processes. These hypotheses for the origins of condition dependency make strongly contrasting and testable predictions about ornamental traits. To assess these two models, we review the mechanisms of production of carotenoids, patterns of condition dependency involving different classes of carotenoids, and patterns of behavioural responses to carotenoid coloration. We review evidence that traits can be condition dependent without the influence of sexual selection and that novel traits can show condition-dependent expression as soon as they appear in a population, without the possibility of sexual selection. We conclude by highlighting new opportunities for studying condition-dependent signalling made possible by genetic manipulation and expression of ornamental traits in synthetic biological systems.
... It is produced by pigments (red keto-carotenoids) whose synthesis could be produced at the core of the cell respiratory function, i.e. into the mitochondrion [6][7][8]. We should first mention that, in many avian species, the red colorations are generated by converting yellow carotenoids acquired with food into red ketocarotenoids [7,9]. That transformation involves redox enzymatic reactions [7,9]. ...
... We should first mention that, in many avian species, the red colorations are generated by converting yellow carotenoids acquired with food into red ketocarotenoids [7,9]. That transformation involves redox enzymatic reactions [7,9]. The cited change is performed by a group of enzymes (ketolases) that seems to be located at the inner mitochondrial membrane (IMM [7,10];). ...
... Leclaire et al. [28] reported a brightness decline in the red bill gape of kittiwakes (a trait also colored by ketocarotenoids: [32]). However, they did not detect changes in the hue or saturation of the gape, which are color parameters linked to tissue carotenoid concentrations [9]. Moreover, the red ketocarotenoids are obtained with food in the seabirds and directly deposited on ornaments without metabolic conversion (reviewed in [9]). ...
Article
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Background The animal signaling theory posits that conspicuous colorations exhibited by many animals have evolved as reliable signals of individual quality. Red carotenoid-based ornaments may depend on enzymatic transformations (oxidation) of dietary yellow carotenoids, which could occur in the inner mitochondrial membrane (IMM). Thus, carotenoid ketolation and cell respiration could share the same biochemical pathways. Accordingly, the level of trait expression (redness) would directly reveal the efficiency of individuals’ metabolism and, hence, the bearer quality in an unfalsifiable way. Different avian studies have described that the flying effort may induce oxidative stress. A redox metabolism modified during the flight could thus influence the carotenoid conversion rate and, ultimately, animal coloration. Here, we aimed to infer the link between red carotenoid-based ornament expression and flight metabolism by increasing flying effort in wild male common crossbills Loxia curvirostra (Linnaeus). In this order, 295 adult males were captured with mist nets in an Iberian population during winter. Approximately half of the birds were experimentally handicapped through wing feather clipping to increase their flying effort, the other half being used as a control group. To stimulate the plumage regrown of a small surface during a short time-lapse, we also plucked the rump feathers from all the birds. Results A fraction of the birds with fully grown rump feathers (34 individuals) could be recaptured during the subsequent weeks. We did not detect any significant bias in recovery rates and morphological variables in this reduced subsample. However, among recaptured birds, individuals with experimentally impaired flying capacity showed body mass loss, whereas controls showed a trend to increase their weight. Moreover, clipped males showed redder feathers in the newly regrown rump area compared to controls. Conclusions The results suggest that wing-clipped individuals could have endured higher energy expenditure as they lost body mass. Despite the small sample size, the difference in plumage redness between the two experimental groups would support the hypothesis that the flying metabolism may influence the redox enzymatic reactions required for converting yellow dietary carotenoids to red ketocarotenoids.
... Plumage colourations come in two different forms; pigment-based colours and structural colours (Maia, D'Alba & Shawkey, 2011). Pigment based colours consist of carotenoids and melanins, which result from a wavelength-dependant absorbance of light (Maia et al., 2011;McGraw, 2006). Carotenoid pigments are acquired from diet and provide warm colours such as yellows, oranges and reds (Goodwin, 1984;Guay, Potvin & Robinson, 2012;McGraw, 2006). ...
... Pigment based colours consist of carotenoids and melanins, which result from a wavelength-dependant absorbance of light (Maia et al., 2011;McGraw, 2006). Carotenoid pigments are acquired from diet and provide warm colours such as yellows, oranges and reds (Goodwin, 1984;Guay, Potvin & Robinson, 2012;McGraw, 2006). In contrast, melanin pigments are synthesized, giving rise to dark colours which are made up of eumelanin (black) and phaeomelanin (brown) (Guay et al., 2012;McGraw, 2006). ...
... Carotenoid pigments are acquired from diet and provide warm colours such as yellows, oranges and reds (Goodwin, 1984;Guay, Potvin & Robinson, 2012;McGraw, 2006). In contrast, melanin pigments are synthesized, giving rise to dark colours which are made up of eumelanin (black) and phaeomelanin (brown) (Guay et al., 2012;McGraw, 2006). In contrast, structural colours refract light, producing coherent scattering of incident light (Maia et al., 2011). ...
Thesis
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Flight feathers are crucial for foraging, predator avoidance and large-scale movements in most avian populations. However, the structural integrity of these feathers can be compromised by growth defects, negatively impacting flight ability and survival. Poor feather condition is characterised by the presence of fault bars, which are weak areas displayed as translucent bands that appear through the width of the feather vane. Fault bars occur as a result of stressful or adverse environmental conditions during feather growth. The thesis investigated the macroscopic and microscopic characteristics of this growth defect in relation to current formation theories, assessed different feather quality measures and explored possible causes and consequences of fault bars. The study was carried out at RSPCA Stapeley Grange Wildlife Centre, which receive a large number of carrion crow Corvus corone admissions displaying poor feather condition each year. Firstly, the macroscopic and microscopic characteristics of fault bars were observed, reviewing existing fault bar formation theories and imagery with the use of advanced technology. Unique observational evidence was presented from this, identifying a ‘squeezed’ appearance to the barbules within fault bars, supporting the hypothesis of muscular constriction around the growing feather pin. Moreover, for the first time, images of fault bar occurrence within the growing feather pin were presented. Relationships between different measures of feather quality were then assessed, accounting for differences between feather type (primary, secondary and tail), in reference to the ‘fault bar allocation’ hypothesis (Jovani & Blas, 2004). In this, fault bars occur on feathers that are least important for flight, resulting in the majority of fault bars being located on the tail feathers, with the lowest numbers in the primary feathers. A variety of feather quality measures were assessed here, including the number of fault bars, average width of fault bars, feather iridescence and strength, in addition to the number of snapped and white feathers. A key finding in this study was the relationship between the average width of fault bars and average feather iridescence across all feather types. This information strengthens our knowledge of how dull feather portray honest communication signals of low fitness. Moreover, average feather strength was found to be an independent measure of quality, with generally no relationship found with other measures of quality. Average fault bar width measurements were used to investigate the causes of fault bar production in relation to chemical profile of feathers, parasite burden, sex and age (study aim 3). This made a valuable and novel discovery, identifying a possible link between calcium deficiency and fault bar occurrence. Calcium an essential element in skeletal mineralisation and eggshell formation. Therefore, the results of this study add to the knowledge of calcium and its role in fitness, expanding to feather quality. This study also found a potential trade-off between costly immune defences facilitated at the cost of feather quality, where low numbers of endoparasite species associated with wide fault bars in the wing feathers. Poor feather quality was not found to vary between sexes, as carrion crows are monomorphic and non-migratory. In regard to age differences, the tail feathers of younger individuals were found to have the widest fault bars. This supports many other studies in highlighting the vulnerability of juveniles during the feather growth period. Lastly, average feather strength measurements were used to investigate the consequences of poor feather quality in relation to the chemical profile of feathers, endoparasite burden, sex and age (study aim 4). A key finding here was that stress resistant bases were associated with a high proportion of chlorine in primary flight feathers. Links to parasite burden and sex were not identified; however, in line with the above findings, younger individuals were found to have low stress tolerance in the primary feathers compared to adults. Differences in feather strength in relation to fault bar occurrence was also reviewed. Contrary to predictions, no differences in strength were found between feather regions with fault bar occurrence and those with fault bar absence. Future research in this field could be extended to nestlings, an age group that was unfortunately excluded from this study due to the presentation of pin feathers. Moreover, research could also be broadened to additional species, as fault bars are found to impact a wide variety of passerine and non-passerine individuals. This may then open opportunities in understanding stressors faced by vulnerable species, aiding future conservation efforts.
... Animal colourations are mainly originated by the synthesis and/or accumulation of pigments [10][11][12][13] or by physical properties of animal integuments that affect reflectance of light when interacting with biological nanostructures (structural colouration) [14]. Yet colourations may also be modified by certain animal behaviours. ...
... Pigments in the uropygial secretion might be synthesized de novo in the gland cells [28] or in other body parts and then transported to the gland, as it occurs with pigments found on the eggshells [30]. They might also come from pigments synthesized by plants or invertebrates that birds incorporate through their diet in the uropygium [10]. Finally, we here hypothesize that pigments in the uropygial secretion may also be derived from the metabolism of symbiotic microorganisms growing within the uropygial gland of birds. ...
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The use of cosmetic substances in communication is widespread in animals. Birds, for instance, use their uropygial secretion as a cosmetic in scenarios of sexual selection and parent-offspring communication. This secretion harbours symbiotic bacteria that could mediate the synthesis of pigments for cosmetic colouration. Here, we investigate the association between bacteria and the conspicuous yellow secretion used by spotless starling (Sturnus unicolor) nestlings to stain their mouths, and hypothesize a possible role of bacteria in the colour production. We also experimentally explore how nestling oxidizing condition influences the microbiota, suggesting that the possible bacterial-mediated coloured secretion acts as a reliable honest signal. An antioxidant supplementation experiment, previously known to affect secretion and mouth colouration, was conducted to assess its impact on the microbial community of secretions from control and experimental siblings. Antioxidant supplementation increased richness and phylogenetic diversity of the secretion’s microbiota. Moreover, the microbiota’s alpha and beta diversity, and the abundance of two bacterial genera (Parabacteroides and Pseudogracilibacillus), correlated with secretion colour. These findings demonstrate that antioxidant condition influences the gland microbiota of starling nestlings, and suggest a link between bacteria and the colouration of their cosmetic secretion. Alternative explanations for the detected links between bacteria and colouration are discussed.
... In addition, carotenoids include many types of compounds. Yellow carotenoids (xanthophylls) are commonly acquired with the diet and directly deposited on ornament tissues (McGraw 2006). In contrast, red carotenoids (ketocarotenoids) are obtained from enzymatic transformations of dietary yellow carotenoids (McGraw 2006;Hill and Johnson 2012). ...
... Yellow carotenoids (xanthophylls) are commonly acquired with the diet and directly deposited on ornament tissues (McGraw 2006). In contrast, red carotenoids (ketocarotenoids) are obtained from enzymatic transformations of dietary yellow carotenoids (McGraw 2006;Hill and Johnson 2012). This transformation seems to be made into the inner mitochondrial membrane (Johnson and Hill 2013;Hill et al. 2019). ...
Article
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Harsh early environmental conditions can exert delayed, long-lasting effects on phenotypes, including reproductive traits such as sexual signals. Indeed, adverse early conditions can accelerate development, increasing oxidative stress that may, in turn, impact adult sexual signals. Among signals, colourations produced by red ketocarotenoids seem to depend on mitochondrial functioning. Hence, they could reveal individual cell respiration efficiency. It has been hypothesized that these traits are unfalsifiable "index" signals of condition due to their deep connection to individual metabolism. Since mitochondrial dysfunction is frequently linked to ageing, red ketocarotenoid-based ornaments could also be good signals of a critical fitness component: longevity. We tested this red colour per longevity correlation in captive zebra finches. In addition, we experimentally decreased the synthesis of glutathione (a critical intracellular antioxidant) during the first days of the birds’ life to resemble harsh early environmental conditions (e.g. undernutrition). Longevity was recorded until the death of the last bird (almost nine years). Males, but not females, exhibiting a redder bill in early adulthood lived longer than males with paler bills, which agrees with some precedent studies. However, such bill redness - longevity connection was absent among males with inhibited glutathione synthesis. These findings may suggest that environmental factors can alter the reliability of red ketocarotenoid-based sexual signals, making them less unfalsifiable than believed.
... lutein and zeaxanthin), or undergo metabolic conversion, either by dehydrogenation into 'canary xanthophylls' (a group of yellow pigments including canary xanthophyll A, B and anhydrolutein) or by 4-oxidation into red keto-carotenoids (e.g. echinenone, adonirubin, astaxanthin;McGraw, 2006c). It has been proposed that ornaments with converted carotenoids exhibit higher condition dependence due to a tight link between the efficiency of cellular processes and pigment metabolism. ...
... lutein or zeaxanthin), while others are metabolically modified before deposition (i.e. dehydrogenated into yellow xanthophylls or hydroxylated into red ketocarotenoids) (McGraw, 2006c). A meta-analysis by Weaver et al. (2018) concluded that converted carotenoids might be more reliable signals of parasite resistance or reproductive quality than dietary carotenoids. ...
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Brilliant, diverse colour ornaments of birds were one of the crucial cues that led Darwin to the idea of sexual selection. Although avian colouration plays many functions, including concealment, thermoregulation, or advertisement as a distasteful prey, a quality-signalling role in sexual selection has attracted most research attention. Sexually selected ornaments are thought to be more susceptible to external stressors than naturally selected traits, and as such, they might be used as a test for environmental quality. For this reason, the last two decades have seen numerous studies on the impact of anthropogenic pollution on the expression of various avian colour traits. Herein, we provide the first meta-analytical summary of these results and examine whether there is an interaction between the mechanism of colour production (carotenoid-based, melanin-based and structural) and the type of anthropogenic factor (categorised as heavy metals, persistent organic pollutants, urbanisation, or other). Following the assumption of heightened condition dependence of ornaments under sexual selection, we also expected the magnitude of effect sizes to be higher in males. The overall effect size was close to significance and negative, supporting a general detrimental impact of anthropogenic pollutants on avian colouration. In contrast to expectations, there was no interaction between pollution types and colour-producing mechanisms. Yet there were significant differences in sensitivity between colour-producing mechanisms, with carotenoid-based colouration being the most affected by anthropogenic environmental disturbances. Moreover, we observed no significant tendency towards heightened sensitivity in males. We identified a publication gap on structural colouration, which, compared to pigment-based colouration, remains markedly understudied and should thus be prioritised in future research. Finally, we call for the unification of methods used in colour quantification in ecological research to ensure comparability of results among studies.
... In the particular case of carotenoids-which are not synthesized by the body-they must be acquired based on dietary intake (Hill, 2000;McGraw, 2006); implying effort in the search for this resource. Given the energetic cost of displaying these colors (Hill, 2000;Moller et al., 2000;McGraw et al., 2005) and the intraspecific color differences that occur (Hill, 2000;Siefferman and Hill, 2003); the classical perspective of the resource trade-off hypothesis considers the expression of carotenoid-based coloration to be a sign of health condition and individual quality (Hill, 2000;McGraw and Ardia, 2004;Hill and McGraw, 2006). ...
... Although it has been reported from human observations that the female is duller than the male in crown color (Hilty and Brown, 2001;Rising et al., 2011), it is unknown if there are quantitative colors differences between sexes of the Saffron Finch in the tropics, and if so, whether these differences are used for recognition between individuals. Most researches addressing this issue has focused on species from North America and Europe (Hill, 1990;McGraw andHill, 2000a, 2000b;Delhey, 2005) with few studies on species from tropical areas (Tubaro et al., 2005;Bridge et al., 2008;Masello et al., 2009;Diniz et al., 2016). Due to the fact that an objective analysis of color and its possible ecological implications in terms of life history has not been carried out in the flaveola group, our objective was to determine, for the first time in the north of South America, whether there are in fact differences in plumage color between individuals and if these differences allow them to discriminate by sex among their congeners. ...
Article
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Sexual dichromatism, a particular type of sexual dimorphism, occurs in several species and has been associated with sexual selection. In some cases, the differences are so small that they are imperceptible to humans, but possibly detected by birds. The objective measurement of color with spectrophotometers and detailed analyses according to the perception ability of the avian eye have revealed that some species that were once considered to be monochromatic, are in fact dichromatic and able to perceive these differences. In the tropics, the Saffron Finch (Sicalis flaveola) does not present marked sexual dimorphism in coloration, which makes studies in behavioral ecology, natural history and population dynamics difficult. To assess whether there is dichromatism in the species, the reflectance (between 300 and 700 nm) of ten body regions was measured in 196 wild adults in Cali-Colombia. Sex was determined using the CHD1 gene on the sex chromosomes. Reflectance spectra were analyzed using: colorimetric variables and the avian visual model. We found that reflectance shows a bimodal curve in all body regions, except the crown. Males presented higher reflectance at long wavelengths, while for females this occurred in ultraviolet wavelengths. For the visual model, we found that there are significant intrasexual differences; however only in crown coloration is there a possible perceived difference between sexes. We conclude that in the Saffron Finch there are color differences between the sexes in all regions considering the physical phenomenon (reflectance), but in general, when evaluating color perception (avian visual model), there are no differences between the sexes in most of the body regions. The intrasexual differences are significant, indicating the possibility of these being signals that influence social interactions in the species.
... Carotenoid pigments are obtained by diet and cannot be synthesized by birds (Goodwin 1992;Funk and Taylor 2019), conferring yellow, orange, and red colors to the plumages (Weaver et al. 2018). Carotenoids are related to individual physiological state and quality, such as the resistance to parasites and immunocompetency (Folstad and Karter 1992;Peters et al. 2004a, b;Butler and McGraw 2013), level of oxidative stress (von Schantz et al. 1999) and foraging capacity (Hill 1992;McGraw 2006). The signal honesty of carotenoid-based plumage ornamentation can be conferred physiologically by a trade-off in allocating carotenoid pigments to self-maintenance (reducing oxidative stress and improving immunocompetency) and plumage ornamentation (the resource allocation trade-off hypothesis) (Alonso- Alvarez et al. 2008;Koch and Hill 2018), or because carotenoidbased plumage shares a pathway with mitochondrial energy metabolism (Powers et al. 2022). ...
... From the second or third breeding season onwards, older females develop the definitive plumage, which is dark yellow (Silveira and Méndez 1999;Sick 2001;Marques-Santos et al. 2018). Such plumage coloration is given by carotenoid pigment lutein (McGraw 2006). Based on plumage coloration, we classified the individuals of S. f. brasiliensis into three plumage color classes: yellow male (i.e., adult males exhibiting yellow plumages), yellow female (i.e., adult females exhibiting dark yellow plumages), or dull birds (i.e., juveniles or subadults of both sexes exhibiting delayed dull plumages). ...
Article
The status signaling hypothesis suggests that inconspicuous plumages are an honest signal of subordination in social animals, including those exhibiting delayed plumage maturation. In addition, body size may also determine the outcome of aggressive interactions and shape dominance relationships. We observed flocks of Saffron Finches (Sicalis flaveola brasiliensis) during the non-breeding season to investigate whether the probability of winning an aggressive interaction varies according to the plumage color class (yellow female, yellow male, and dull bird of both sexes), morphology (body mass, wing length, and tail length), and plumage color variation (reflectance of yellow breast feathers). In this subspecies, younger individuals of both sexes breed with duller plumage and present late maturation to yellow, definitive plumage. We found that, in general, yellow females were more likely to win aggressive interactions against conspecifics (of any plumage color class) than yellow males and dull birds, irrespective of plumage color variation or morphology. In contrast, yellow males were not more likely to win aggressive interactions against conspecifics than dull birds. When comparing yellow females to each other and yellow males to each other, in general, larger birds and birds with brighter plumages were more likely to win the aggressive interactions. Our results partially support the status signaling hypothesis, suggesting that plumage color class has a major influence on social dominance status, whereas gradual variation in morphology and plumage coloration signals fighting ability within plumage color classes.
... Traditionally, two arguments have been made to link variation in carotenoid-based colour and individual quality. First, because birds cannot synthesise carotenoids de novo, they need to ingest them with their food (McGraw, 2006). This led to the hypothesis that carotenoid-based coloration may signal foraging ability, especially if carotenoids are limited in the environment. ...
... Carotenoids are the second most common pigment in birds after melanin (Delhey, 2015;McGraw, 2006), and our survey confirms that in the largest avian radiation, the passerines, yellow carotenoid-based plumage colours are much more common than red (Delhey & Peters, 2017;Olson & Owens, 2005). We show that passerines with red carotenoid-based plumage had longer carotenoid metabolism pathways than species with only yellow, confirming the common assumption that red carotenoid-based colours are more likely to result from carotenoid metabolization (Delhey & Peters, 2017;Hill, 1996;Prasetya et al., 2020). ...
Article
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Many birds use carotenoids to colour their plumage yellow to red. Because birds cannot synthesise carotenoids, they need to obtain these pigments from food, although some species metabolise dietary carotenoids (which are often yellow) into derived carotenoids (often red). Here, we study the occurrence of yellow and red carotenoid‐based plumage colours in the passerines, the largest bird radiation and quantify the effects of potential ecological and life‐history drivers on their evolution. We scored the presence/absence of yellow and red carotenoid‐based plumage in nearly 6,000 species and use Bayesian phylogenetic mixed models to assess the effects of carotenoid‐availability in diet, primary productivity, body size, habitat and sexual selection. We also test the widespread assumption that red carotenoid‐based colours are more likely to be the result of metabolization. Finally, we analyse the pattern of evolutionary transitions between yellow and red carotenoid‐based plumage colours to determine whether, as predicted, the evolution of yellow carotenoid‐based colours precedes red. We show that, as expected, both colours are more likely to evolve in smaller species and in species with carotenoid‐rich diets. Yellow carotenoid‐based plumage colours, but not red, are more prevalent in species that inhabit environments with higher primary productivity and closed vegetation. In general, females were more likely to have yellow and males more likely to have red carotenoid‐based plumage colours, closely matching the effects of sexual selection. Our analyses also confirm that red carotenoid‐based colours are more likely to be metabolised than yellow carotenoid‐based colours. Evolutionary gains and losses of yellow and red carotenoid‐based plumage colours indicate that red colours evolved more readily in species that already deposited yellow carotenoids, while the reverse was rarely the case. Our study provides evidence for a general, directional evolutionary trend from yellow to red carotenoid‐based colours, which are more likely to be the result of metabolization. This may render them potentially better indicators of quality, and thus favoured by sexual selection.
... Accordingly, sexual ornamentation and other sexual signals are frequently exaggerated (e.g., in their size, vividness of color, etc.) beyond that required for effective signal transmission and detection, perhaps because exaggeration can increase signaling costs and provide more reliable information on individual quality (Tazzyman et al. 2014). For example, carotenoid-based color ornaments are often discussed as sexual signals that, due to resource limitation or to physiological costs, can honestly convey information on individual quality (Olson and Owens 1998;McGraw 2006; but see also Simons et al. 2012;Koch and Hill 2018). ...
... Carotenoid-based colors were proposed to be costly because carotenoids are obtained exclusively from the diet, rather than synthesized by animals, and may therefore be a limiting resource (McGraw 2006). In addition, since carotenoids serve physiological functions related to immune and antioxidant defense (Lozano 1994;von Schantz et al. 1999), their allocation to coloration could also compromise physiological condition (meta-analysis in Simons et al. 2012). ...
Article
Sexual ornamentation is often assumed to be costly, allowing honest signaling of individual quality, and carotenoid-based colors were proposed to bear significant costs. If carotenoid-based colors are costly to produce, sexually-selected signals should use more concentrated carotenoid pigments and have more saturated color than non-sexual signals, where honesty-guaranteeing costs are not required. We tested this prediction comparing carotenoid-based colors across canaries, goldfinches and allies, because many of these species use yellow plumage as sexual ornamentation, but also have yellow rumps that appear to be non-sexual flash marks. Only in the breast, but not the rump, was there an asymmetric co-distribution of male and female color saturation, with males similarly or more saturated than females, indicating evolution of breast color by sexual selection. Yellow was not consistently more saturated in the breast than in the rump, and the co-distribution of rump and breast color saturation indicated that saturated rumps can persist irrespective of breast color. This challenges the assumption that carotenoid-based colors bear significant costs. The use of carotenoid coloration as sexual signals in this clade may instead be due to social costs, cost-free index mechanisms for signaling quality, and/or socially-monogamous species evolving low-cost signals to mostly discriminate against low-quality mates.
... Vertebrates, including lizards, employ two distinct pigment types to generate sexual coloration, and these may be differentially influenced by urbanization (Mc-Graw 2006a,b). Coloration based on carotenoids cannot be produced endogenously by vertebrates and must be acquired through diet, making it a reliable indicator of body condition and foraging efficiency (McGraw 2006a;Biard et al. 2017). In contrast, structural (or melanin) coloration can be synthesized endogenously by animals and is considered less condition-dependent and more genetically controlled than carotenoid coloration (McGraw 2006b;Roulin 2016). ...
Article
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Urbanization is a global phenomenon that involves the transformation of natural areas into urban spaces, thereby subjecting organisms to new selective pressures including a wide variety of pollutants and changes in intra‐ and interspecific interactions. Considering that projections indicate that by the year 2050, 65% of the human population will live in urban areas and that urbanization is a phenomenon with an upward pattern, identifying these phenotypic traits is vital to implementing conservation and management plans for urban fauna. The urban environment may exert different selective pressures on sexually selected traits than more pristine environments, a phenomenon which has been well studied in birds but is less understood in other vertebrates such as lizards, although they are common inhabitants of urban environments. Here, we compare sexual coloration, parasite load, and immune response in Sceloporus torquatus lizards in urban and non‐urban environments of Central Mexico. Our study shows that sexual coloration is more saturated (bluer) in male lizards from urban environments, while UV chroma was higher in non‐urban lizards. The average parasite load is lower in urban lizards than in non‐urban lizards, and we found a negative relationship between hemoparasite count and sexual coloration in male lizards from non‐urban environments but not in male lizards from urban environments. Additionally, non‐urban lizards exhibited a higher immune response. In female lizards, sexual coloration differed significantly between urban and non‐urban environments, but parasite load and immune response did not differ. These results may be useful to improve herpetofauna conservation plans in urbanized environments.
... Experimental studies have 50 demonstrated that carotenoid-based coloration can be sensitive to hormone 51 manipulation (Khalil et Thompson et al., 1997), and stress induced by captivity (Hill, 1992). The sensitivity of 54 ornamental coloration to environmental stress has been found to be particularly striking 55 for species that metabolically modify dietary carotenoids before they are used in 56 ornaments (Brush, 1990;Mcgraw, 2006). Indeed, a meta-analysis investigating the 57 strength of condition dependency of carotenoid-based ornaments in songbirds found 58 that, relative to ornaments produced with dietary carotenoids, ornaments that required 59 metabolized carotenoids were more reliable signals of condition (Weaver et al., 2018). ...
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In many species of animals, red carotenoid-based coloration is produced by metabolizing yellow dietary pigments, and this red ornamentation is an honest signal of individual quality. However, the physiological basis for associations between organism function and the metabolism of red ornamental carotenoids from yellow dietary carotenoids remains uncertain. A recent hypothesis posits that carotenoid metabolism depends on mitochondrial performance, with diminished red coloration resulting from altered mitochondrial aerobic respiration. To test for an association between mitochondrial respiration and red carotenoids, we held wild-caught, molting male house finches in either small bird cages or large flight cages to create environmental challenges during the period when red ornamental coloration is produced. We predicted that small cages would present a less favorable environment than large flight cages and that captivity would affect both mitochondrial performance and the abundance of red carotenoids. We found no evidence that living in small versus large cages had significant effects on wild-caught house finches; however, birds in cages of any size circulated fewer red carotenoids, showed increased mitochondrial respiratory rates, and had lower complex II respiratory control ratios—a metric associated with mitochondrial efficiency—compared to free-living birds. Moreover, among captive individuals, the birds that circulated the most red carotenoids had the highest mitochondrial respiratory control ratio for complex II substrates. These data support the hypothesis that the metabolism of red carotenoid pigments is linked to mitochondrial aerobic respiration in the house finch, but the mechanisms for this association remain to be established. SUMMARY STATEMENT Holding wild-caught male house finches in cages exposed a relationship between red carotenoid production and mitochondrial respiratory efficiency.
... With respect to red carotenoid pigmentation, the degree of pathway similarity among species is unclear, as red carotenoids can be either sequestered directly from the diet or metabolically converted from yellow dietary carotenoids (McGraw 2006;Toomey et al. 2022). With metabolic conversion, a ketolase enzyme essentially builds upon the existing carotenoid pathway to add a novel function, although different animal groups Downloaded from https://academic.oup.com/sysbio/advance-article/doi/10.1093/sysbio/syad051/7240510 by guest on 10 November 2023 appear to use different, but related, enzymes. ...
Article
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Convergent evolution is defined as the independent evolution of similar phenotypes in different lineages. Its existence underscores the importance of external selection pressures in evolutionary history, revealing how functionally similar adaptations can evolve in response to persistent ecological challenges through a diversity of evolutionary routes. However, many examples of convergence, particularly among closely related species, involve parallel changes in the same genes or developmental pathways, raising the possibility that homology at deeper mechanistic levels is an important facilitator of phenotypic convergence. Using the genus Ranitomeya, a young, color-diverse radiation of Neotropical poison frogs, we set out to (1) provide a phylogenetic framework for this group, (2) leverage this framework to determine if color phenotypes are convergent, and (3) to characterize the underlying coloration mechanisms to test whether color convergence occurred through the same or different physical mechanisms. We generated a phylogeny for Ranitomeya using ultraconserved elements and investigated the physical mechanisms underlying bright coloration, focusing on skin pigments. Using phylogenetic comparative methods, we identified several instances of color convergence, involving several gains and losses of carotenoid and pterin pigments. We also found a compelling example of nonparallel convergence, where, in one lineage, red coloration evolved through the red pterin pigment drosopterin, and in another lineage through red ketocarotenoids. Additionally, in another lineage, "reddish" coloration evolved predominantly through structural color mechanisms. Our study demonstrates that, even within a radiation of closely related species, convergent evolution can occur through both parallel and nonparallel mechanisms, challenging the assumption that similar phenotypes among close relatives evolve through the same mechanisms.
... Within the framework of host-parasite interactions, much attention has been given to the connection between parasites and sexually selected traits, as these characters have been hypothesized to be particularly sensitive to parasites, acting as reliable signals of health status (Hamilton & Zuk, 1982). Most research in this sense has focused on carotenoid-based colorations, which are paradigms of sexually selected traits (McGraw, 2006). This is because carotenoids, which can only be acquired through diet, are often a limited resource and their use for pigmenting teguments must be traded off with other potential functions of these molecules, such as acting as immunostimulants or antioxidants in the organism (Chew & Park, 2004;Lozano, 1994;P erez Rodr ıguez, 2009). ...
Article
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A central issue in avian ecology deals with the trade‐off between investment life‐history components, such as reproductive effort, and parasite and disease resistance. During reproduction, differences in the particular needs of males and females may further affect the outcome of such trade‐off. However, most studies performed to date on avian species have focused on males, while less is known about this subject in females. We investigated haemoparasite infections (genera Haemoproteus, Plasmodium and Leucocytozoon) in relation to sex, year, body condition and plasma concentrations of carotenoids in wild‐breeding Red‐legged partridges (Alectoris rufa). Our aim was to examine whether there are differences in infections between sexes and how parasite infections relate to carotenoid levels, physical condition and breeding parameters in non‐passerine wild birds. Males captured early in the breeding season were in better body condition than females, indicating a marked sexual difference in this trait in wild Red‐legged partridges. The prevalence of blood parasites in males was higher than in females. However, we found that females infected by blood parasites had lower plasma carotenoid concentrations than uninfected females, whereas no association between infection and carotenoid levels was found in males. This suggests sex‐related differences in the use of carotenoids to fight infections or for parasite resistance. A possible explanation of this contrasting pattern between sexes is that reproduction may not have to involve the same costs for males and females. We suggest that males would be under strong sexual selection and would trade health for signalling, which could simultaneously explain highest parasite prevalence being found in males and the contrasting patterns in blood carotenoid levels between males and females. Females in contrast, that were in worst body condition during early breeding season, were more sensitive to infections, diverting carotenoids to immune function more than males.
... For the purposes of this article, sexual selection's implications for coloration primarily apply to avian species, because most mammalian species are not sexually dimorphic in color ( Price 2006, McPherson and Chenoweth 2012, Cooney et al. 2019 . Although many of the colors that are under sexual selection in birds are carotenoid based and derived from diet rather than melanin based ( McGraw 2006 ) , there are a few examples of altered sexual selection of melanin-based coloration in urban areas. Great tits ( Parus major ) in Barcelona, Spain, were found to have smaller black ties than forest birds. ...
Article
With novel human–wildlife interaction, predation regimes, and environmental conditions, in addition to often fragmented and smaller populations, urban areas present wildlife with altered natural selection parameters and genetic drift potential compared with nonurban regions. Plumage and pelage coloration in birds and mammals has evolved as a balance between avoiding detection by predator or prey, sexual selection, and thermoregulation. However, with altered mutation rates, reduced predation risk, increased temperatures, strong genetic drift, and increased interaction with people, the evolutionary contexts in which these colorations arose are radically different from what is present in urban areas. Regionally alternative color morphs or leucistic or melanistic individuals that aren't typical of most avian or mammalian populations may become more frequent as a result of adaptive or neutral evolution. Therefore, I conceptualize that, in urban areas, conspicuous color morphologies may persist, leading to an increase in the frequency of regionally atypical pelage coloration. In the present article, I discuss the potential for conspicuous color morphs to arise and persist in urban mammalian and avian populations, as well as the mechanisms for such persistence, as a result of altered environmental conditions and natural selection pressures.
... In this work, we will talk about the two most common classes of pigments (melanins and carotenoids) (McGraw, 2003(McGraw, , 2003aStoddard and Prum, 2011). In passerine birds (order Passeriformes), only and exclusively these pigments (bur often in a combination with the feather structure) determine the entire color palette of the plumage. ...
Article
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In passerine birds, the coloration of plumage is associated with two groups of pigments (melanins and carotenoids). The physiological bases of the appearance of melanin-and carotenoid-based coloration are fundamentally different, and these types of coloration reflect different characteristics of an individual. It is considered that the expressiveness of melanin-based coloration primarily depends on genetic factors, while the expressiveness of carotenoid-based coloration depends on the state and health of an individual at the moment. Therefore, the individual variability of these two types of coloration should be independent of each other. We studied the coloration of the second (from the distal edge) rectrix in 109 greenfinch males of two age cohorts (one year old and aged two or more years). The relationship between the level of aggressiveness of different birds and their color characteristics was also considered. The feathers we are interested in are two-color; their distal part is black (or blackish), while the proximal part (basis) is yellow. The black color is caused by melanins, while the yellow one by carotenoids. We demonstrated that the saturation of yellow carotenoid-based coloration in greenfinch males has a significant and negative relationship with the length of the black (melanin) spot on the same rectrix (the relationship of the saturation of the yellow coloration with the length of the yellow field is, respectively, positive). Thus, the individual variability of melanin-and carotenoid-based coloration in our case is parallel. This indicates that the roles of these groups of pigments as indicators (mark-ers) of the quality and state of an individual were not as fundamentally different as is commonly thought. However, there are definitely differences in this regard between melanin-and carotenoid-based coloration: the black melanin-based coloration in the greenfinch is associated with aggressiveness, while the yellow carotenoid-based one is not.
... In recent years, the classic 'resource allocation' models of avian carotenoid honesty have given way to an emphasis on the metabolism of carotenoids [7,9], in particular the ability of several species to produce red ketocarotenoids (KCs) by C4-oxygenation (ketolation) of the yellow carotenoids that are common in avian diets [10][11][12][13]. There are several potential mechanisms by which the rate or efficiency of ketolation might link coloration to some phenotypic or genetic quality; for example, if the ketolation is energetically demanding, entails oxidative stress or is linked to 'vital cellular processes' [14], such as vitamin A homeostasis [9], detoxification ability [15] or cellular respiration [16]. ...
Article
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Intense red colours in birds are often owing to ketocarotenoids (KCs). In many land birds, KCs are oxidized from dietary yellow precursors, presumably by the avian carotenoid ketolase CYP2J19, the regulation and constraints of which have important implications for condition-dependence and honest signalling of carotenoid colour displays. We investigated hepatic CYP2J19 gene expression in the seasonally and sexually dichromatic southern red bishop ( Euplectes orix ) in relation to season, sex, progression of the prenuptial moult, testis size, body condition, redness and circulating sex steroids. A coloration function of CYP2J19 is supported by a seasonal upregulation prior to and during the carotenoid-depositing stage of the male prenuptial moult. However, CYP2J19 expression was similarly high in females (which do not moult prenuptially), and remained high in males after moult, suggesting additional or alternative roles of hepatic CYP2J19 or its products, such as detoxification or antioxidant functions. In males, the CYP2J19 upregulation preceded and was unrelated to the rise in plasma testosterone, but was correlated with androstenedione, probably of adrenal origin and compatible with luteinizing hormone-induced and (in females) oestrogen-suppressed moult. Finally, contrary to ideas that carotenoid ketolation rate mediates honest signalling of male quality, CYP2J19 expression was not related to plumage redness or male body condition.
... Carotenoids, which produce yellow, orange and red coloration, are among the main pigments in the plumage of many bird species (Fox, 1979;McGraw, 2006). These pigments are produced by bacteria, plants and fungi and, as most animals cannot synthesise them, must be ingested with food (Fox, 1979). ...
Article
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It has been proposed that carotenoid-based pigmentation should indicate the ability of individuals to acquire food and that this should be reflected in their body condition. In this study we examined whether the body condition of Greater Flamingos Phoenicopterus roseus was related to plumage coloration and the interaction of both variables with sex and foraging site. To this end, we conducted a field study to collect data on sex-related body condition and plumage coloration at two wetlands in southern Spain. We found that body condition was site-related, that the more colourful individuals were in better body condition, and that females were more colourful and in better body condition than males. Together, the results suggest that females have greater need than males to signal individual quality, likely because females encounter higher intraseasonal costs than males during reproduction, and choosing low-quality females could severely limit breeding success. Also, plumage coloration may signal individual status at foraging sites throughout the year.Amat, J.A., Garrido, A., Rendn-Martos, M., Portavia, F. & Rendn, M.A. (2022). Plumage coloration in Greater Flamingos Phoenicopterus roseus is affected by interactions between foraging site, body condition and sex. Ardeola, 69: 219-229. Se ha propuesto que la pigmentacin basada en carotenoides indicara la habilidad de los individuos para obtener alimento y que ello se reflejara en su condicin corporal. En este estudio examinamos si la condicin corporal del flamenco comn Phoenicopterus roseus estuvo relacionada con la coloracin del plumaje, as como la interaccin de ambas variables con el sexo y el sitio de alimentacin. Para ello realizamos un estudio de campo, durante el cual tomamos datos sobre condicin corporal y color del plumaje en relacin al sexo en dos humedales del sur de Espaa. Encontramos que la condicin corporal estuvo relacionada con el sitio, que los individuos ms coloridos presentaron una condicin corporal mejor y que las hembras fueron ms coloridas y con una condicin corporal mejor en comparacin a los machos. En conjunto, los resultados sugirieron que las hembras tendran una necesidad mayor que los machos para sealizar la calidad individual, probablemente porque las hembras asumen dentro de la poca de reproduccin unos costes mayores que los machos, de forma que las hembras de baja calidad podran limitar severamente el xito de cra. Adems, la coloracin del plumaje podra sealizar el estatus individual en las zonas de alimentacin a lo largo del ao.Amat, J.A., Garrido, A., Rendn-Martos, M., Portavia, F. y Rendn, M.A. (2022). La coloracin del plumaje en los flamencos comunes Phoenicopterus roseus est afectada por interacciones entre el sitio de alimentacin, la condicin corporal y el sexo. Ardeola, 69: 219-229.
Article
Animal populations can exhibit dramatic variation in individual fitness, and microbiota are emerging as a potentially understudied factor influencing host health. Bacterial diversity and community structure of the gut microbiome are associated with many aspects of fitness in animals, but relatively little is known about the generality of these relationships in wild populations and non‐mammalian taxa. We studied the northern cardinal Cardinalis cardinalis , a member of a taxon that is ecologically important but underrepresented in microbiome research: songbirds. To test for relationships between the microbiota and host fitness, we sampled the cloacal microbiomes of wild cardinals and measured body condition index, assessed coloration of sexual ornaments (beak and plumage), and collected blood to estimate the glucocorticoid response to stress. Both alpha and beta bacterial diversity were related to individual variation in body condition and several sexual ornaments, but not glucocorticoid concentrations. Our results from a free‐living songbird population add to a growing body of research linking avian host fitness to internal bacterial community characteristics. This study sets the stage for manipulative experiments to determine how challenges to fitness and microbiomes may upset these relationships.
Article
Coloured patches of skin are seen across the animal kingdom and serve multiple functions. For many species, carotenoid pigments are often incorporated into the skin, hair or feathers and feature prominently in colourful signals used as sexual signals. Most animals cannot synthesise carotenoids de novo and, as a result, carotenoid-based signals have long been considered indicators of individual quality. We identified and quantified the carotenoids within the eye combs of black grouse (Lyrurus tetrix) using ultrahigh performance liquid chromatography–mass spectrometry. We found that black grouses incorporate two ketocarotenoids, astaxanthin and canthaxanthin, into their eye combs in different proportions depending on total eye comb size, with individuals with smaller combs incorporating significantly more canthaxanthin than astaxanthin. Additionally, a higher ratio of astaxanthin to canthaxanthin significantly decreased brightness, but was positively associated with both the λUV peak and the λR peak. The results found here highlight the need to also consider the additional effects of tissue structure on carotenoid, and overall colouration.
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The carotenoid-based colors of birds are a celebrated example of biological diversity and an important system for the study of evolution. Recently, a two-step mechanism, with the enzymes cytochrome P450 2J19 (CYP2J19) and 3-hydroxybutyrate dehydrogenase 1-like (BDH1L), was described for the biosynthesis of red ketocarotenoids from yellow dietary carotenoids in the retina and plumage of birds. A common assumption has been that all birds with ketocarotenoid-based plumage coloration used this CYP2J19/BDH1L mechanism to produce red feathers. We tested this assumption in house finches ( Haemorhous mexicanus ) by examining the catalytic function of the house finch homologs of these enzymes and tracking their expression in molting birds. We found that CYP2J19 and BDH1L did not catalyze the production of 3-hydroxy-echinenone (3-OH-echinenone), the primary red plumage pigment of house finches, when provided with common dietary carotenoid substrates. Moreover, gene expression analyses revealed little to no expression of CYP2J19 in liver tissue or growing feather follicles, the putative sites of pigment metabolism in molting house finches. Finally, although the hepatic mitochondria of house finches have high concentrations of 3-OH-echinenone, observations using fluorescent markers suggest that both CYP2J19 and BDH1L localize to the endomembrane system rather than the mitochondria. We propose that house finches and other birds that deposit 3-OH-echinenone as their primary red plumage pigment use an alternative enzymatic pathway to produce their characteristic red ketocarotenoid-based coloration.
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Parents invest in their progeny to increase offspring survival, ultimately maximizing their own fitness. However, this investment is limited and this leads to the emergence of evolutionary conflicts of interest (i.e., sexual, parent-offspring and sibling conflict), as the different family members may disagree on how resources are distributed. Historically, theoretical models assumed that parental care strategies are fixed and that they can only change over evolutionary timescales. Yet more recent models rather specified rules for responding to the behaviour of partners and offspring in behavioural timescales. These models assume that individuals may negotiate until reaching a settlement, which implies that their fitness-related decisions are flexible and can be modulated according to the information on offer. The acquisition of information then again requires communication, which could be facilitated through informative signals that can be either static (e.g., plumage colouration) or plastic (e.g., offspring begging behaviour). However, we currently know too little about how flexible parental response rules are and to what extent individual responses and the flexibility in behavioural strategies are affected by signaling traits, in a context with multiple senders and receivers – the family. The main objective of this thesis was therefore to study (a) flexibility in care strategies and how this relates to resource allocation trade-offs and the environmental context, and (b) how optimal care strategies are modulated by signals as expressed by the family. Using blue tits (Cyanistes caeruleus) as a model system, we tested the hypothesis that signals expressed by family members facilitate flexible response rules (“negotiation”) over parental care in different contexts (e.g., physical or social environment). First, I investigated how the trade-off between current reproduction and self-maintenance is modulated by the availability of a key resource, lutein, during egg laying. Here I found that enhanced lutein availability increased female egg laying capacity, but at the cost a thinner egg shell. Possibly because the supplementation of this carotenoid pigment interfered with the calcium acquisition and deposition. Then, I investigated whether blue tit parents adjust their feeding strategies to the expression of an offspring signalling trait, and how changes in parental strategies depend on the quality of the environment (i.e., the manipulation of carotenoid availability; or family size). Parents should invest equally in all their offspring under good conditions (i.e., enhanced female intrinsic capacity, or once the initial brood size is reduced), when their rearing capacity allow them to raise all the brood. In contrast, they should shift their investment towards the offspring with the highest probability of survival when parental capacities are too limited (i.e., when the initial brood size is enlarged). Such parental favouritism could be facilitated through the expression of condition-dependent signalling traits that may inform parents about offspring quality (i.e., ultraviolet (UV)/yellow breast feathers of blue tit nestlings). Offspring UV colouration mediated intra-family interactions, and this effect depended on the quality of the prenatal environment and the brood demand. Fathers favoured UV-blocked nestlings when their female partner was lutein-supplemented during egg laying, and hence possibly in a better condition. Parents preferentially fed offspring signalling lower quality (UV-blocked) when their rearing capacities were sufficient to raise all nestlings reduced broods. Then, I investigated the function of the same colouration in blue tit adults. Parental feedings increased in nests in which the UV reflectance was experimentally reduced in one of the parents. This increase was due to the fact that partners of UV-blocked adults enhanced the number of feedings, presumably to compensate the lower-quality appearance of their mates. UV-blocked adults did not change their own rate of nestling provisioning. However, offspring did not respond to the parental manipulated signal, which contradicted my hypothesis that parental signals would simultaneously matter for multiple intra-family contexts. Ultimately, if parental feeding decisions are guided by the expression of signals, the offspring plumage colouration could be a condition-dependent trait that allows parents to distinguish their offspring quality. Here, I found that the total reflectance of yellow breast feathers could act as an honest signal during intra-family interactions, since it varied with body mass within broods. Interestingly, this colour parameter, and the reflectance in the UV region reflected brood quality (e.g., rearing capacity, genetic or environmental effects). The function of this pattern is as yet unclear. These results reveal a significant flexibility in behavioural strategies within the context of parental care. Family signals would facilitate flexible behavioural responses, which are dependent on the context. All family members responded (although to a different extent) to the experimental manipulation of different environmental factors or signalling traits that determine the information provided in the family environment. Yet signalling may facilitate the flexibility and hence diversity of fitness-related decisions taken by the different family members, which may allow them to reach a settlement that optimises trade-offs along a negotiation continuum.
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Carotenoid-dependent ornaments can reflect animals’ diet and foraging behaviors. However, this association should be spatially flexible and variable among populations to account for geographic variation in optimal foraging behaviors. We tested this hypothesis using populations of a marine predator (the brown booby, Sula leucogaster) that forage across a gradient in ocean depth in and near the Gulf of California. Specifically, we quantified green chroma for two skin traits (foot and gular color) and their relationship to foraging location and diet of males, as measured via global positioning system tracking and stable carbon isotope analysis of blood plasma. Our three focal colonies varied in which foraging attributes were linked to carotenoid-rich ornaments. For gular skin, our data showed a shift from a benthic prey-green skin association in the shallow waters in the north to a pelagic prey-green skin association in the deepest waters to the south. Mean foraging trip duration and distance of foraging site from coast also predicted skin coloration in some colonies. Finally, brown booby colonies varied in which trait (foot versus gular skin color) was associated with foraging metrics. Overall, our results indicate that male ornaments reflect quality of diet and foraging–information that may help females select mates who are adapted to local foraging conditions and therefore, are likely to provide better parental care. More broadly, our results stress that diet-dependent ornaments are closely linked to animals’ environments and that we cannot assume ornaments or ornament signal content are ubiquitous within species, even when ornaments appear similar among populations.
Article
In many species of animals, red carotenoid-based coloration is produced by metabolizing yellow dietary pigments, and this red ornamentation can be an honest signal of individual quality. However, the physiological basis for associations between organism function and the metabolism of red ornamental carotenoids from yellow dietary carotenoids remains uncertain. A recent hypothesis posits that carotenoid metabolism depends on mitochondrial performance, with diminished red coloration resulting from altered mitochondrial aerobic respiration. To test for an association between mitochondrial respiration and red carotenoids, we held wild-caught, molting male house finches in either small bird cages or large flight cages to create environmental challenges during the period when red ornamental coloration is produced. We predicted that small cages would present a less favorable environment than large flight cages and that captivity itself would decrease both mitochondrial performance and the abundance of red carotenoids compared to free-living birds. We found that captive-held birds circulated fewer red carotenoids, showed increased mitochondrial respiratory rates, and had lower complex II respiratory control ratios—a metric associated with mitochondrial efficiency—compared to free-living birds, though we did not detect a difference in the effects of small cages versus large cages. Among captive individuals, the birds that circulated the highest concentrations of red carotenoids had the highest mitochondrial respiratory control ratio for complex II substrate. These data support the hypothesis that the metabolism of red carotenoid pigments is linked to mitochondrial aerobic respiration in the house finch, but the mechanisms for this association remain to be established.
Article
The topographical, geological, climatic and biodiversity complexity of Mesoamerica has made it a primary research focus. The Mesoamerican highlands is a region with particularly high species richness and within-species variation. The Cinnamon-bellied Flowerpiercer, Diglossa baritula (Wagler, 1832), is a species endemic to the Mesoamerican highlands, with three allopatric subspecies currently recognized. To characterize divergence within this species, we integrated genomics, morphology, coloration and ecological niche modeling approaches, obtained from sampling individuals across the entire geographic distribution of the species. Our results revealed a clear genomic divergence between the populations to the east versus the west of the Isthmus of Tehuantepec. In contrast to the genomic results, morphology and coloration analyses showed intermediate levels of differentiation, indicating that population groups within D. baritula have probably been under similar selective pressures. Our morphology results indicated that the only sexually dimorphic morphological variable is the wing chord, with males having a longer wing chord than females. Finally, ecological data indicated that there are differences in ecological niche within D. baritula . Our data suggest that D. baritula could contain two or more incipient species at the intermediate phase of the speciation continuum. These results highlight the importance of the geographical barrier of the Isthmus of Tehuantepec and Pleistocene climatic events in driving isolation and population divergence in D. baritula . The present investigation illustrates the speciation potential of the D. baritula complex and the capacity of Mesoamerican highlands to create cryptic biodiversity and endemism.
Article
Birds display a rainbow of eye colours, but this trait has been little studied compared with plumage coloration. Avian eye colour variation occurs at all phylogenetic scales: it can be conserved throughout whole families or vary within one species, yet the evolutionary importance of this eye colour variation is under‐studied. Here, we summarize knowledge of the causes of eye colour variation at three primary levels: mechanistic, genetic and evolutionary. Mechanistically, we show that avian iris pigments include melanin and carotenoids, which also play major roles in plumage colour, as well as purines and pteridines, which are often found as pigments in non‐avian taxa. Genetically, we survey classical breeding studies and recent genomic work on domestic birds that have identified potential ‘eye colour genes’, including one associated with pteridine pigmentation in pigeons. Finally, from an evolutionary standpoint, we present and discuss several hypotheses explaining the adaptive significance of eye colour variation. Many of these hypotheses suggest that bird eye colour plays an important role in intraspecific signalling, particularly as an indicator of age or mate quality, although the importance of eye colour may differ between species and few evolutionary hypotheses have been directly tested. We suggest that future studies of avian eye colour should consider all three levels, including broad‐scale iris pigment analyses across bird species, genome sequencing studies to identify loci associated with eye colour variation, and behavioural experiments and comparative phylogenetic analyses to test adaptive hypotheses. By examining these proximate and ultimate causes of eye colour variation in birds, we hope that our review will encourage future research to understand the ecological and evolutionary significance of this striking avian trait.
Chapter
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This chapter uses research with various canary relatives to explain the use of song and colour ornamentation as communication signals, especially in the contexts of mate choice, agonistic competition, mate guarding and stimulation. As a result of their social and sexual functions, song and colour diverged greatly between species, often evolving in directions that indicate aspects of individual quality. Comparing song and colouration among the canary relatives, accounting for their pattern of common ancestry, uncovered interesting and even novel evolutionary phenomena. For example, it has been found that several species evolved physiologically demanding songs, pushing limits of syllable complexity, that female colouration evolved by a combination of genetic correlation with males plus female-specific evolution, and that divergence in colour facilitates the origin of new species.
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Avian plumage coloration could be altered by external factors like dust accumulation, but the effect of environmental conditions on such post-moult colour changes are poorly studied. Here, we investigated how exposure to the atmosphere in habitats of differing anthropogenic pressures modifies UV/blue structural plumage coloration — a sexually selected trait in eastern bluebirds Sialia sialis. We collected feather samples from live birds and distributed them in three types of habitats: (i) urban roads with low traffic, (ii) urban roads with high traffic, and (iii) rural roads with low traffic. After 4 weeks, the brightness of feathers decreased in all types of habitats-resulting in less-ornamented coloration. Changes in UV and blue chroma, however, varied with habitat type; chroma decreased in urban areas (becoming less ornamented), but increased in rural locations (becoming more ornamented). According to physiological models of avian colour vision, however, these changes in coloration tended to be below perceptual thresholds. Our results underscore the importance of how human activity can influence plumage colour of individual birds during the period between moult cycles which could have an impact on avian visual signalling. The study opens venues for further studies focusing on how the optical properties of specific airborne particles can influence coloration of wild-living animals. Significance statement Plumage coloration plays an important role in avian visual communication. In addition to moult-based change, coloration may change between moult cycles due to exposure to external factors like, for example, dust accumulation. Ecological factors modifying a passive plumage change, however, remains poorly studied. We collected samples of structurally coloured feather from a species wherein plumage colour is sexually selected and exposed them to outdoor conditions. We demonstrate that UV/blue chroma of coloration changes differently in urban and rural habitats. It increased in rural and decreased in urban areas. On the other hand, brightness decreased in both habitat types. Using physiological models of avian colour vision, however, we found that these colour changes were likely not perceptible to birds. Our study provides the first evidence that changes in coloration of fully grown feathers may be habitat dependent.
Chapter
The skin of birds keeps out pathogens and other potentially harmful substances, retains vital fluids and gases, serves as a sensory organ, and produces and supports feathers. This chapter describes the structure of avian skin and explains the functions of unfeathered areas of skin found in some species of birds, like vultures. Interspecific variation in the structure of avian claws and rhamphotheca and the factors that contribute to such variation are discussed. Next, the structure and function of specialized structures like wattles and combs are explained, as are the structure and function of integument glands. Next, the evolution of feathers is discussed, and the structure and function of the different types of feathers are described. Also described in detail is skin and feather color, including the role of pigments and structure. Colors produced by thin- and multi-film interference and photonic structures are also explained. The chapter closes with a discussion of feather parasites and the defenses used by birds to combat those parasites.
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Understanding the causes and limits of phenotypic diversification remains a key challenge in evolutionary biology. Color patterns are some of the most diverse phenotypes in nature. In birds, recent work within families has suggested that plumage complexity might be a key innovation driving color diversity. Whether these patterns hold at larger taxonomic scales remains unknown. Here, we assemble a large database of UV-Vis spectral data across five diverse clades of birds (45791 spectra, 1135 species). Using multivariate phylogenetic comparative methods, we compare evolutionary rates and color space occupancy (i.e., quantification of observed colors) among these clades. Novel color-producing mechanisms have enabled clades to occupy new regions of color space, but using more coloration mechanisms did not result in overall more color space occupancy. Instead, the use of more color-producing mechanisms resulted in faster rates of color evolution and less integrated color among plumage regions. Flexible Bayesian modeling further allowed us to assess the relationship between interpatch and interspecific directions of color variation. We find that interpatch variation generally diverges from interspecies cladewise trends in males but not females, suggesting developmental or selective constraints operating in females across evolutionary scales. By comparing rates among clades and assessing both interpatch and interspecies color variation, we reveal how innovations and constraints operate across evolutionary and developmental scales.
Article
The immense diversity of plumage coloration exhibited by birds is the result of either pigments deposited in the feathers or microstructural arrangements of feather barbules. Some of the most common pigments are carotenoids, which produce bright yellow, orange, and red colors. Carotenoids differ from other pigments since birds cannot synthesize them de novo and must obtain them from the diet. Carotenoid pigments are usually associated with signaling and sexual selection, although they also have antioxidant properties and play a role in the immune response. Here, we hypothesize that carotenoid-dependent plumage coloration functions as a signal of a male’s tendency to invest in offspring care because they play an important role in self-maintenance and may provide key information about individual quality; allowing females to obtain information about a male’s tendency to invest in offspring care. Using phylogenetic comparative analyses across 349 passerine birds, we show that species that consume carotenoid-rich foods have more carotenoid-dependent plumage coloration than species with carotenoid-poor diets. In addition, carotenoid-dependent plumage coloration is associated with decreased male investment in offspring care. Our results suggest that investment in carotenoid-dependent plumage coloration trades off against male investment in offspring care and will likely have broad implications for our understanding of the ecological contexts that facilitate various evolutionary processes, such as sexual selection and signaling associated with plumage colors.
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The domestic canary (Serinus canaria) is one of the most common pet birds and has been extensively selected and bred over the last few centuries to constitute many different varieties. Plumage pigmentation is one of the main phenotypic traits that distinguish canary breeds and lines. Feather colours in these birds, similarly to other avian species, are mainly depended on the presence of two major types of pigments: carotenoids and melanins. In this study, we exploited whole genome sequencing (WGS) datasets produced from five canary lines or populations (Black Frosted Yellow, Opal, Onyx, Opal × Onyx and Mogno, some of which carrying different putative dilute alleles), complemented with other WGS datasets retrieved from previous studies, to identify candidate genes that might explain pigmentation variability across canary breeds and varieties. Sequencing data were obtained using a DNA pool‐seq approach and genomic data were compared using window‐based FST analyses. We identified signatures of selection in genomic regions harbouring genes involved in carotenoid‐derived pigmentation variants (CYP2J19, EDC, BCO2 and SCARB1), confirming the results reported by previous works, and identified several other signatures of selection in the correspondence of melanogenesis‐related genes (AGRP, ASIP, DCT, EDNRB, KITLG, MITF, MLPH, SLC45A2, TYRP1 and ZEB2). Two putative causative mutations were identified in the MLPH gene that may explain the Opal and Onyx dilute mutant alleles. Other signatures of selection were also identified that might explain additional phenotypic differences between the investigated canary populations.
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Avian plumage coloration could be altered by external factors like dust accumulation, but the effect of environmental conditions on such post-moult colour changes are poorly studied. Here, we investigated how exposure to the atmosphere in habitats of differing anthropogenic pressures modifies UV/blue structural plumage coloration- a sexually-selected trait in Eastern Bluebirds Sialia sialis . We collected feather samples from live birds and distributed them in three types of habitats: i) urban roads with low traffic, ii) urban roads with high traffic, iii) rural roads with low traffic. After 4 weeks, the brightness of feathers decreased in all types of habitats-resulting in less-ornamented coloration. Changes in UV and blue chroma, however, varied with habitat type; chroma decreased in urban areas (becoming less ornamented), but increased in rural locations (becoming more ornamented). According to physiological models of avian colour vision, however, these changes in coloration tended to be below perceptual thresholds. Our results underscore the importance of how human activity can influence plumage colour of individual birds during the period between moult cycles which could have an impact on avian visual signaling. The study opens venues for further studies focusing on how the optical properties of specific airborne particles can influence coloration of wild-living animals.
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The last decade a couple of observations of melanistic greater flamingos have been reported across Southern Mediterranean region. In October 2014 a melanistic greater flamingo was observed and photographed for the first time in Europe in Lake Kerkini National Park in Northern Greece. All the decade's observations could concern the same individual if we considered that melanism is an extremely rare genetic mutation and flamingos are moving across different lakes around the Mediterranean region.
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Female ornamentation is frequently observed in animal species and is sometimes found as more evolutionary labile than male ornamentation. A complex array of factors may explain its presence and variation. Here we assessed the role of female cost of reproduction and paternal care. Both factors have been pinpointed as important by theoretical studies but have not been investigated yet in details at the interspecific level. We worked on 133 species of North temperate Passeriformes bird species for which both the clutch volume – here taken as the proxy of female cost of reproduction – and amount of paternal care are relatively well known. Using spectrometry, we measured the whole-body coloured plumage patches and quantified three metrics corresponding to brightness (i.e. achromatic component), colour chromaticity (i.e. intensity) and colour volume (i.e. diversity). We found a strong association between male and female colour metrics. Controlling for this association, we found additional small but detectable effects of both cost of reproduction and paternal care. First, females of species with more paternal care were slightly brighter. Second, the interaction between the level of paternal care and egg volume was correlated with female colour intensity: females with more paternal care were more chromatic, with this association mostly present when their investment in reproduction was low. Together these results suggest that female cost of reproduction and paternal care are part of the multiple factors explaining variation of female coloration, besides the strong covariation between male and female coloration. Abstract To a lesser extent than male conspicuous plumage, female plumage colouration may also vary across bird species. This study explores the role of egg production and male parental care in the evolution of female plumage colouration, using 133 species of songbirds. Pictures were provided by Justine Le Vaillant, David López-Idiáquez and Matthew Silk.
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The immense diversity of plumage coloration exhibited by birds is the result of either pigments deposited in the feathers or microstructural arrangements of feather barbules. Some of the most common pigments are carotenoids that produce bright yellow, orange and red colors. Carotenoids differ from other pigments since birds cannot synthesize them de novo and must obtain them from the diet. Carotenoid pigments are usually associated with signaling and sexual selection, although they also have antioxidant properties and play a role in the immune response. Here we hypothesize that carotenoid-dependent plumage coloration functions as a signal of a male's tendency to invest in offspring care because they play an important role in the self-maintenance and may provide key information about individual quality; allowing females to obtain information about a males' tendency to invest in offspring care. Using phylogenetic comparative analyses across 350 passerine birds we show that species that consume carotenoid-rich foods have more carotenoid-dependent plumage coloration than species with carotenoid-poor diets. In addition, carotenoid-dependent plumage coloration is associated with a decreased male investment in offspring care. Our results suggest investment into carotenoid-dependent plumage coloration trades off against male investment into offspring care and will likely have broad implications for our understanding of the ecological contexts that facilitate various evolutionary processes such as sexual selection or signaling associated with plumage colors.
Article
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Carotenoids are diet-based micronutrients important in health and coloration signaling. Related species with similar diets can differ in the kinds and levels of circulating carotenoids, which suggests specific physiological mechanisms to efficiently utilize these micronutrients, regardless of their availability. We explored whether diet and parental provisioning of unusual sources of carotenoids (fresh vegetal matter and vertebrate feces) can explain the occurrence and concentrations of carotenoids in the cinereous vulture Aegypius monachus, griffon vulture Gyps fulvus, and Egyptian vulture Neophron percnopterus nestlings, even when these pigments appear to not be deposited in their integumentary system. A greater diversity of wild prey in diet could be behind the profile of higher concentrations of carotenoids in the Egyptian vulture, the species with carotenoid-dependent coloration during adulthood, while differences in diet composition between cinereous and griffon vultures do not translate to different carotenoid profiles. The carotenoid profile appears to not be related to the ingestion of unusual matter rich in these compounds, although the infrequent occurrence of lycopene and an unidentified γ-carotene-like compounds suggest that these vultures may be exploiting vegetal matter that left no identifiable unconsumed remains in the nest of Egyptian vultures. The consumption of green plant material by griffon vultures does not result in especially high levels of carotenoids when compared to the carotenoids found in cinereous vultures, which do not consume green plant material. Ungulate feces were not provisioned to Egyptian vulture nestlings, despite the fact they contain carotenoids that adults need for appropriate coloration. Overall, this study indicates that diet differences alone appear insufficient to explain contrasting inter-specific carotenoid profiles, especially since all types of food consumed are considered to be poor in carotenoids, except vegetable matter. We suggest that nestling Egyptian vultures are comparatively efficient in up taking carotenoids present in low concentrations in food when these compounds are not deposited in their integument, which suggests allocation to other functions.
Article
Male Painted Buntings (Passerina ciris) display at least 6 distinct plumage colors that encapsulate much of the visible light spectrum, yet the specific mechanisms responsible for generating this diversity of color have not been identified. Here, we show that metabolically derived carotenoids and nanostructures capable of producing structural color were ubiquitous across feather patches. We used digital photography, light microscopy, spectrophotometry, carotenoid extraction, and high-performance liquid chromatography to show that the resulting color of each feather patch depended on the concentration of carotenoids, melanins, and underlying feather nanostructures. For example, we found that the blue-violet head feathers contained low concentrations of ketolated carotenoids, which is not typical of blue-violet structurally colored feathers. Additionally, the red breast and orange belly feathers contained a green tuned structural color visible after carotenoid extraction, which is not typical of feathers that contain ketolated carotenoids. Although, none of these abnormal combinations of carotenoids and structural coloration appeared to significantly impact feather color. Conversely, we found the purple rump, dark green greater coverts, and bright yellow-green mantle feather coloration resulted from the combination of high concentrations of carotenoids and the presence of structural color. For the first time, we identify the combination of red ketolated carotenoids and blue structural color as a mechanism to produce purple feather coloration. Identifying the specific mechanisms that give rise to the diversity of colors within this species will facilitate the study of the—to date—unknown signaling functions of colors produced through the combination of carotenoids and nanostructures in Painted Buntings and other songbirds.
Article
Female birds allocate high concentrations of biologically active carotenoid pigments to their egg yolks, which help to protect developing embryos against damage from free radicals and increase the rates of nestling survival after hatching. In most avian species studied to date, carotenoids are allocated in higher concentrations to the first-laid egg and lower to the last-laid egg in the laying sequence, which has been attributed to a limitation of carotenoids in avian diets. We studied laying-sequence variation in carotenoid concentrations and egg metrics (i.e., egg mass, yolk mass, shell mass, egg length, and egg width) in 15 full clutches of House Sparrow (Passer domesticus) eggs collected from nest boxes on the main campus of Columbus State University, in Columbus, Georgia, during the breeding seasons of 20142018. We identified 4 yellow dietary carotenoids in House Sparrow egg yolks, -carotene, -cryptoxanthin, lutein, and zeaxanthin, with lutein being the most highly concentrated. We found that concentrations of most carotenoids significantly decreased from first- to last-laid eggs, but we did not find significant differences in any egg metrics across the laying sequence. To our knowledge, this research is the first to report detailed information on laying-sequence variation in yolk carotenoids in House Sparrow eggs, making our results an important contribution to the understanding of variation in the allocation of carotenoids to songbird eggs. Las hembras de las aves asignan altas concentraciones de pigmentos carotenoides biolgicamente activos a las yemas de sus huevos, las cuales ayudan a proteger los embriones en desarrollo de los daos ocasionados por radicales libres e incrementan las tasas de sobrevivencia de los polluelos despus de la eclosin. En la mayora de las especies de aves que se han estudiado hasta la fecha, los carotenoides son asignados en mayores concentraciones al primer huevo de la puesta y sta disminuye hasta el ltimo huevo en la secuencia de la puesta, lo cual ha sido atribuido a una limitacin en los carotenoides en las dietas de los pjaros. Estudiamos la variacin en concentracin de carotenoides y mtricas de los huevos segn la secuencia de puesta (i.e., masa del huevo, masa de la yema, masa del cascarn, longitud del huevo y ancho del huevo), en 15 puestas completas de huevos del gorrin domstico (Passer domesticus) colectadas de cajas-nido en el campus principal de la Columbus State University en Columbus, Georgia, durante las temporadas reproductivas de 20142018. Identificamos 4 carotenoides de dieta en las yemas de los huevos del gorrin domstico, -caroteno, -criptoxantina, lutena y zeaxantina, siendo la lutena la ms altamente concentrada. Encontramos que las concentraciones de la mayora de los carotenoides decrecieron significativamente del primer al ltimo huevo de la puesta, aunque no encontramos diferencias significativas en ninguna de las mtricas de los huevos a lo largo de la secuencia de puesta. De lo que sabemos, esta investigacin es la primera que reporta informacin detallada de la variacin en carotenoides segn la secuencia de puesta en huevos del gorrin domstico, lo que hace de nuestros resultados una importante contribucin al entendimiento de la variacin en la asignacin de carotenoides en los huevos de aves canoras. Palabras clave: -caroteno, especies invasoras, intra-puesta, lutena, yema de huevo.
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In many vertebrates, the enzymatic oxidation of dietary yellow carotenoids generates red keto‐carotenoids giving color to ornaments. The oxidase CYP2J19 is here a key effector. Its purported intracellular location suggests a shared biochemical pathway between trait expression and cell functioning. This might guarantee the reliability of red colorations as individual quality signals independent of production costs. We hypothesize that the ornament type (feathers vs. bare parts) and production costs (probably CYP2J19 activity compromising vital functions) could have promoted tissue‐specific gene relocation. We review current avian tissue‐specific CYP2J19 expression data. Among the ten red‐billed species showing CYP2J19 bill expression, only one showed strong hepatic expression. Moreover, a phylogenetically‐controlled analysis of 25 red‐colored species shows that those producing red bare parts are less likely to have strong hepatic CYP2J19 expression than species with only red plumages. Thus, both production costs and shared pathways might have contributed to the evolution of red signals. Ketocarotenoid pigments synthesized from dietary yellow carotenoids produce red colorations in many vertebrates. In birds, this transformation can be made peripherally (integument) or centrally (hepatic conversion). We hypothesize that this depends on the ornament type (plumage vs. bare parts) following a pattern that avoids production costs.
Article
Sexual selection research has long focused on the evolution of female mate preferences. Most of the models that have been developed posit that mate preferences evolve in a mating context. In contrast, the sensory bias model proposes that mate choice preferences arise in a non-mating context, as a by-product of natural selection acting on a female’s perceptual system. Recent research has shown that many species of fishes, from across a large clade including poeciliids, goodeids, and medaka, have a bias for long wavelength (LW) colors (yellow, orange, red) in a non-mating context. Even species that do not have LW-colored ornaments, apparently because they have been lost secondarily, retain this latent bias for LW colors. Here, we predicted that female Oryzias latipes (Japanese medaka), a drab species with a latent preference for LW colors, would show a mate choice preference for males with an artificial secondary sexual trait—a colored stripe added to their flank. We confirmed that females were more responsive to red and orange objects in a non-mating context than to other colors. We also showed that females were less resistant towards males with an LW-colored stripe than to those enhanced with a non-LW stripe and that, for many females, responses towards specific LW colors were consistent across these non-mating and mating contexts. Therefore, our results provide support for the sensory bias model by providing a link between a sensory bias in a non-mating context and a mate choice preference in a drab species like medaka.
Chapter
The red-legged partridge is increasingly recognized as a good study model in ecophysiology and evolutionary biology. Most research in these fields has focused on the expression of coloured social signals. The fact that this species expresses the two main types of coloured ornaments among vertebrates (i.e. carotenoid- and melanin-based) has attracted the interest of scientists investigating the mechanisms behind the function and evolution of these traits. Intensive research on the colour of the beak, eye rings and legs of this species has revealed that the redness of these characters results from the accumulation of two main carotenoids (astaxanthin and papilioerythrinone) that the animal synthesizes at the integument from dietary precursors. Diet composition, intestinal parasites, body condition, oxidative stress and androgen levels significantly affect the expression of the characteristic redness of these traits, making them reliable indicators of individual quality. Melanin-based plumage ornaments of the red-legged partridge (black bib and barred flank feathers) have been relatively less studied. However, experimental studies have shown that their expression is connected to the oxidative status of the individual during feather growth. In addition, the pattern of the black bib —measured through its fractal dimension— is sensitive to the body condition of the individual during moult. Given that most of these studies have been performed in captivity, the main challenge in the short term is to validate and calibrate the conclusions obtained in captivity with studies performed in the wild. This would also help evaluate the interconnection among different signalling traits —including behavioural displays— and their relative importance under different social and environmental contexts.
Article
Plumage coloration can have substantial effects on a bird's energy budget. This is because different colours reflect and absorb light differently, affecting the heat loads acquired from solar radiation. We examine the thermal effects of feather coloration on solar heat gain and flight performance and discuss the potential role of plumage colour on a bird's energy budget. Early investigations of the effects of plumage colour on thermoregulation revealed complex interactions between environmental conditions and physical properties of the plumage that may have led to diverse behavioural and physiological adaptations of birds to their thermal environment. While darker feather surfaces absorb more light, and heat more, than light‐coloured surfaces under exposure to the sun, this relationship is not always straightforward when considering heat transfer to the skin. Heat transfer through plumage varies depending on multiple factors, such as feather density and transmission of light. For instance, higher transmissivity of light‐coloured plumage can increase heat loads reaching skin level, while conduction and convection transfer heat from the surface of dark feathers to the skin. Solar heating can affect the metabolic costs of maintaining a constant body temperature, and depending on environmental conditions, colours can have either a positive or negative effect on a bird's energy budget. More specifically, solar heating can be advantageous in the cold but may increase the energetic costs associated with thermoregulation when ambient temperature is high. More recent studies have further suggested that the thermal properties of feather coloration might reduce the energetic costs of flight. This is because surface heating can affect the ratio between lift and drag on a wing. As concluding remarks, we provide future directions for new lines of research that will aid in improving our understanding of the thermal effects of feather coloration on a bird's energy budget, which can potentially explain factors driving colour evolution and distribution patterns in birds.
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We investigated potential information content in red carotenoid-based undertail coverts of 28 pairs of breeding Great Spotted Woodpeckers by comparing plumage reflectance to measures of body condition and reproductive success. Plumage coloration was not significantly associated with sex or age, and did not correlate with body condition or the number of offspring fledged. Further, we found no evidence of assortative mating related to plumage colour. Our research provides an example of an exception from the commonly held hypothesis that carotenoid-based plumage coloration signals individual condition. Future surveys incorporating other plumage traits and physiological measures of condition in Great Spotted Woodpeckers are needed to verify our findings.
Article
Rapid physiological colour change offers dynamic signalling opportunities that can reveal distinct information to receivers in different contexts. Information content in dynamic colours, however, is largely unexplored. In males of the Indian rock agama (Psammophilus dorsalis), stressful events, including male-male agonistic interactions, induce a colour change, wherein the dorsal band turns yellow and the lateral bands turn orange. We aimed to determine whether these pigment-based dynamic colours convey information about individual quality. Using an agamid-specific visual model, we first quantified the chromatic and achromatic contrasts of each colour component displayed by males during handling stress, which induces the maximal response of aggression-typical colours. We then measured baseline testosterone levels, morphology (body mass and size), and performance measures (bite force and sprint speed) of these lizards. Chromatic contrasts of the dorsal yellow and lateral orange bands, individually and relative to each other (internal pair), were negatively correlated with testosterone levels, while the chromatic contrast of the internal pair was positively correlated with body condition. The lack of an association between colour contrasts and both bite force and sprint speed indicate that the conspicuousness of colours expressed during stressful events, such as agonistic interactions, do not reveal male performance ability. Despite our expectations of a positive relationship with testosterone, morphology (body condition), and performance (bite force, sprint speed), we find that for P. dorsalis, the conspicuousness of stress-induced colours provide only some information about individual quality. We speculate that the dynamicity of physiological colours may influence their function as content-containing signals in social interactions.
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