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publicMay 2020View details →

Origin of the natural variation in the storage of dietary carotenoids in freshwater amphipod crustaceans

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publicJul 2024View details →

Potential for the production of carotenoids of interest in the polar diatom Fragilariopsis cylindrus

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publicMay 2022View details →

Same colors for different functions: implications for the evolution of carotenoid-based ornamentation

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publicNov 2019View details →

Carotenoid- but not melanin-based plumage coloration is negatively related to metal exposure and proximity to the road in an urban songbird

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opencc-zeroAug 2020View details →

Data from: Testosterone regulates CYP2J19-linked carotenoid signal expression in male red-backed fairywrens (Malurus melanocephalus)

Carotenoid pigments produce most red, orange, and yellow colours in vertebrates. This coloration can serve as an honest signal of quality that mediates social and mating interactions, but our understanding of the underlying mechanisms that control carotenoid signal production, including how different physiological pathways interact to shape and maintain these signals, remains incomplete. We investigated the role of testosterone in mediating gene expression associated with a red plumage sexual signal in red-backed fairywrens (Malurus melanocephalus). In this species, males within a single population can flexibly produce either red/black nuptial plumage or female-like brown plumage. Combining correlational analyses with a field-based testosterone implant experiment and qPCR, we show that testosterone mediates expression of carotenoid-based plumage in part by regulating expression of CYP2J19, a ketolase gene associated with ketocarotenoid metabolism and pigmentation in birds. This is the first time that hormonal regulation of a specific genetic locus has been linked to carotenoid production in a natural context, revealing how endocrine mechanisms produce sexual signals that shape reproductive success.

opencc-zeroJan 2021View details →

VCF data file and code for: CYP2J19 mediates carotenoid colour introgression across a natural avian hybrid zone

It has long been of interest to identify the phenotypic traits that mediate reproductive isolation between related species, and more recently, the genes that underpin them. Much work has focused on identifying genes associated with animal colour, with the candidate gene CYP2J19 identified in laboratory studies as the ketolase converting yellow dietary carotenoids to red ketocarotenoids in birds with red pigments. But evidence that CYP2J19 explains variation between red and yellow feather coloration in wild populations of birds is lacking. Hybrid zones provide the opportunity to identify genes associated with specific traits. Here we investigate genomic regions associated with colour in red-fronted and yellow-fronted tinkerbirds across a hybrid zone in southern Africa. We sampled 85 individuals, measuring spectral reflectance of forecrown feathers and scoring colours from photographs, while testing for carotenoid presence with Raman spectroscopy. We performed a genome-wide association study to identify associations with carotenoid-based coloration, using double-digest RAD sequencing aligned to a short-read whole genome of a Pogoniulus tinkerbird. Admixture mapping using 104,933 SNPs identified a region of chromosome 8 that includes CYP2J19 as the only locus with more than two SNPs significantly associated with both crown hue and crown score, while Raman spectra provided evidence of ketocarotenoids in red feathers. Asymmetric backcrossing in the hybrid zone suggests that yellow-fronted females mate more often with red-fronted males than vice versa. Female red-fronted tinkerbirds mating assortatively with red-crowned males is consistent with the hypothesis that converted carotenoids are an honest signal of quality.

Data from: Condition-dependent expression of carotenoid- and melanin-based plumage colour of northern flicker nestlings revealed by manipulation of brood size

Carotenoid-based colouration in feathers is widely accepted to be a reliable signal of the health of an individual, but the condition-dependence of melanin-based plumage ornaments has been highly debated. Using broods that were manipulated in size, we tested whether nutritional stress during rearing affected the carotenoid pigmentation in secondary feathers and the size, shape, and symmetry of melanin spots on breast plumage of northern flicker Colaptes auratus nestlings. Two measures of carotenoid colour (chroma and brightness) of secondary flight feathers did not vary according to brood size treatment, but in a larger dataset from the population, carotenoid chroma was positively associated with nestling mass. Nestlings from experimentally enlarged broods had smaller melanin spots than those from reduced broods, which is some of the first experimental evidence that melanin ornament size in growing nestlings is condition-dependent. However, the shape and symmetry of the melanin breast spots was not associated with nestling mass. Sexual dimorphism was apparent in both types of pigmentation and future studies should investigate whether there are any trade-offs for nestlings between investing in carotenoid colouration and melanisation and whether trade-offs differ between the sexes.

opencc-zeroDec 2010View details →

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

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

Data from: The meaning of melanin, carotenoid, and pterin pigments in the bluefin killifish, Lucania goodei

Male bluefin killifish (Lucania goodei) exhibit extensive color variation in their fins, but the utility of this variation has not yet been determined. We collected males from multiple populations and spectrophotometrically determined the pigment types responsible for fin coloration. We determined that the orange coloration in the caudal fin is caused by carotenoid pigmentation. In contrast, color in the anal fin is either pterin based (yellow and red) or structural (blue) with a melanic fin border. As these colors have different developmental origins, the potential for complex signaling is high. Therefore, we sought to determine whether behavior, reproductive success, or health correlated with pigmentation. Males with more melanin on the anal fin were more dominant and had higher spawning success. Male–male aggression was greater between males with similar-sized melanic borders, indicating that melanic markings function as badges of status between males. Caudal carotenoid pigmentation did not correlate with dominance, but this highly labile ornament was correlated with body condition, parasite infection, and spawning success, suggesting a role in intersexual selection by signaling health to potential mates. Similar results were found for caudal fin coloration using digital photography. Pterin pigmentation in the anal fin was not related to dominance but was related to overall spawning levels and parasite infection, suggesting that pterin pigmentation may also signal immune status. Thus, the coloration of male bluefin killifish provides multiple messages to multiple receivers through these 3 pigments (melanin, pterin, and carotenoid) that have distinct developmental origins.

opencc-zeroJun 2019View details →

Data from: Red carotenoids and associated gene expression explain colour variation in frillneck lizards

A longstanding hypothesis in evolutionary ecology is that red-orange ornamental colours reliably signal individual quality due to limited dietary availability and metabolic costs associated with their production, such as the bio-conversion of dietary yellow carotenoids to red ketocarotenoids. However, in ectothermic vertebrates, these colours can also be produced by self-synthesised pteridine pigments. As a consequence, the relative ratio of pigment types and their biochemical and genetic basis have implications for the costs and information content of colour signals; yet they remain poorly known in most taxonomic groups. We tested whether red and yellow-frilled populations of the frillneck lizard, Chlamydosaurus kingii, differ in the ratio of different biochemical classes of carotenoid and pteridine pigments, and examined associated differences in gene expression. We found that, unlike other squamate reptiles, red hues derive from a higher proportion of ketocarotenoids relative to both dietary yellow carotenoids and to pteridines. Whereas red frill skin showed higher expression of several genes associated with carotenoid metabolism, yellow frill skin showed higher expression of genes associated with steroid hormones. Based on the different mechanisms underlying red and yellow signals, we hypothesise that frill colour conveys different information in the two populations. More generally, the data expand our knowledge of the genetic and biochemical basis of colour signals in vertebrates.

Data from: Nonautosomal genetic variation in carotenoid coloration

Carotenoid-based coloration plays an important role in signaling, is often sexually dimorphic, and is potentially subject to directional and/or sex-specific selection. To understand the evolutionary dynamics of such color traits, it is essential to quantify patterns of inheritance, yet nonautosomal sources of genetic variation are easily overlooked by classical heritability analyses. Carotenoid metabolism has recently been linked to mitochondria, highlighting the potential for color variation to be explained by cytoplasmically inherited factors. In this study, we used quantitative genetic animal models to estimate the importance of mitochondrial and sex chromosome–linked sources of genetic variation in coloration in two songbird populations in which dietary carotenoids are either unmodified (great tit plumage) or metabolized into alternative color forms (zebra finch beak). We found no significant Z-linked genetic variance in great tit plumage coloration, while zebra finch beak coloration exhibited significant W linkage and cytoplasmic inheritance. Our results support cytoplasmic inheritance of color in the zebra finch, a trait based on endogenously metabolized carotenoids, and demonstrate the potential for nonautosomal sources to account for a considerable share of genetic variation in coloration. Although often overlooked, such nonautosomal genetic variation exhibits sex-dependent patterns of inheritance and potentially influences the evolution of sexual dichromatism.

opencc-zeroDec 2018View details →

Data from: Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard

Reptiles use pterin and carotenoid pigments to produce yellow, orange, and red colors. These conspicuous colors serve a diversity of signaling functions, but their molecular basis remains unresolved. Here, we show that the genomes of sympatric color morphs of the European common wall lizard (Podarcis muralis), which differ in orange and yellow pigmentation and in their ecology and behavior, are virtually undifferentiated. Genetic differences are restricted to two small regulatory regions, near genes associated with pterin (SPR) and carotenoid metabolism (BCO2), demonstrating that a core gene in the housekeeping pathway of pterin biosynthesis has been co-opted for bright coloration in reptiles and indicating that these loci exert pleiotropic effects on other aspects of physiology. Pigmentation differences are explained by extremely divergent alleles and haplotype analysis revealed abundant trans-specific allele sharing with other lacertids exhibiting color polymorphisms. The evolution of these conspicuous color ornaments is the result of ancient genetic variation and cross-species hybridization.

opencc-zeroDec 2016View details →

Data from: Maternal allocation of carotenoids increases tolerance to bacterial infection in brown trout

Life-history theory predicts that iteroparous females allocate their resources differently among different breeding seasons depending on their residual reproductive value. In iteroparous salmonids there is typically much variation in egg size, egg number, and in the compounds that females allocate to their clutch. These compounds include various carotenoids whose functions are not sufficiently understood yet. We sampled 37 female and 35 male brown trout from natural streams, collected their gametes for in vitro fertilizations, experimentally produced 185 families in 7 full-factorial breeding blocks, raised the developing embryos singly (n = 2960), and either sham-treated or infected them with Pseudomonas fluorescens. We used female redness (as a measure of carotenoids stored in the skin) and their allocation of carotenoids to clutches to infer maternal strategies. Astaxanthin contents largely determined egg colour. Neither egg weight nor female size was correlated with the content of this carotenoid. However, astaxanthin content was positively correlated with larval growth and with tolerance against P. fluorescens. There was a negative correlation between female skin redness and the carotenoid content of their eggs. Although higher astaxanthin contents in the eggs were associated with an improvement of early fitness-related traits, some females appeared not to maximally support their current offspring as revealed by the negative correlation between female red skin colouration and egg carotenoid content. This correlation was not explained by female size and supports the prediction of a maternal trade-off between current and future reproduction.

Data from: Colour in a new light: a spectral perspective on the quantitative genetics of carotenoid coloration

1. Carotenoid-based colours are model traits for research on animal signalling and sexual selection but, whereas the consequences of variable expression have been extensively studied, its causes are rarely quantified. This issue is complicated by the composite nature of carotenoid-based colour patches, which combine pigments and a reflective background. Ultimately, the evolution of such colours will be determined by the processes that govern variable expression of these mechanisms. 2. We present a novel approach to assessing the quantitative genetics of colour expression, in which reflectance spectra are analysed directly, thereby avoiding the data loss and inherent subjectivity of summary colour variables. Further, the influence of the multiple component mechanisms can be distinguished in spectral analyses due to their contrasting wavelength-dependencies. 3. Using data from a six-year study of carotenoid-based plumage reflectance in wild great tits (Parus major), we employ a multi-parallel 'animal modelling' approach to estimate sources of variance for narrow (2nm) wavebands across the visible spectrum. 4. Moderate heritability estimates were limited to the violet-blue region of the spectrum, diagnostic of the carotenoid content of plumage being heritable. The natal environment effect was limited entirely to the violet-blue, again indicating that it relates to variation in carotenoid content of feathers. Other wavelengths were sensitive to annual and permanent environmental variation but only marginally influenced by additive genetic variation. Hence background reflectance is the component that is more sensitive to the environment. 5. Analysing reflectance spectra directly provided an objective perspective of the dynamics of colour expression that is not apparent when relying on summary colour scores. In this case, our results suggest that carotenoid deposition may be an effective target of selection and hence could explain the important role carotenoids frequently play in intraspecific signalling.

opencc-zeroDec 2016View details →

Data from: Environmental stress linked to consumption of maternally derived carotenoids in brown trout embryos (Salmo trutta)

The yellow, orange, or red colors of salmonid eggs are due to maternally derived carotenoids whose functions are not sufficiently understood yet. Here, we studied the significance of naturally acquired carotenoids as maternal environmental effects during embryo development in brown trout (Salmo trutta). We collected eggs from wild females, quantified their egg carotenoid content, fertilized them in vitro in full-factorial breeding blocks to separate maternal from paternal effects, and raised 3,278 embryos singly at various stress conditions until hatching. We found significant sire effects that revealed additive genetic variance for embryo survival and hatching time. Dam effects were 5.4 times larger than these sire effects, indicating that maternal environmental effects play an important role in determining embryo stress tolerance. Of the eight pigment molecules that we targeted, only astaxanthin, zeaxanthin (that both affected egg redness), and lutein were detected above our confidence thresholds. No strong link could be observed between carotenoid content in unfertilized eggs and embryo mortality or hatching timing. However, the consumption of carotenoids during our stress treatment was negatively correlated to embryo survival among sib groups and explained about 14% of the maternal environmental variance. We conclude that maternally derived carotenoids play a role in the ability of embryos to cope with environmental stress, but that the initial susceptibility to the organic pollution was mainly determined by other factors.

opencc-zeroDec 2017View details →

Data from: Significant differences in maternal carotenoid provisioning and effects on offspring fitness in Chinook salmon colour morphs

In oviparous species, maternal carotenoid provisioning can deliver diverse fitness benefits to offspring via increased survival, growth, and immune function. Despite demonstrated advantages of carotenoids, large intra‐ and interspecific variation in carotenoid utilization exists, suggesting trade‐offs associated with carotenoids. In Chinook salmon (Oncorhynchus tshawytscha), extreme variation in carotenoid utilization delineates two colour morphs (red and white) that differ genetically in their ability to deposit carotenoids into tissues. Here, we take advantage of this natural variation to examine how large differences in maternal carotenoid provisioning influence offspring fitness. Using a full‐factorial breeding design crossing morphs and common‐garden rearing, we measured differences in a suite of fitness‐related traits, including survival, growth, viral susceptibility, and host response, in offspring of red (carotenoid‐rich eggs) and white (carotenoid‐poor eggs) females. Eggs of red females had significantly higher carotenoid content than those of white females (6X more); however, this did not translate into measurable differences in offspring fitness. Given that white Chinook salmon may have evolved to counteract their maternal carotenoid deficiency, we also examined the relationship between egg carotenoid content and offspring fitness within each morph separately. Egg carotenoids only had a positive effect within the red morph on survival to eyed‐egg (earliest measured trait), but not within the white morph. While previous work shows that white females benefit from reduced egg predation, our study also supports a hypothesis that white Chinook salmon have evolved additional mechanisms to improve egg survival despite low carotenoids, providing novel insight into evolutionary mechanisms that maintain this stable polymorphism.

Data from: Oxidative stress is related to both melanin- and carotenoid-based ornaments in the common yellowthroat

Male ornaments are hypothesized to signal the ability of males to produce an effective immune response without extensive oxidative stress and damage to DNA. We examined this hypothesis in male common yellowthroats (Geothlypis trichas), which have two ornaments, a black (eumelanin-based) facial mask and a yellow (carotenoid-based) bib. In our study population, only the black mask is sexually selected. As predicted by the oxidative stress hypothesis, males with larger black masks were more resistant to oxidative stress, as measured by an in vitro assay of the resistance of erythrocytes to haemolysis by free radicals. Furthermore, males with larger masks also tended to have lower levels of glutathione, which was predicted because glutathione inhibits eumelanin production. In contrast, mask size was not related to absolute levels of oxidative stress measured in the plasma. Although the yellow bib is not under sexual selection in our population, males with larger bibs and feathers with greater carotenoid chroma had lower levels of oxidative stress. The oxidative stress hypothesis was first proposed for carotenoid-based ornaments. However, our results suggest that, even in the same individuals, carotenoid and eumelanin-based plumage ornaments may both signal the ability of males to resist or manage oxidative stress.

Data from: Carotenoid-based bill coloration functions as a social, not sexual, signal in songbirds (Aves: Passeriformes)

Many animals use coloration to communicate with other individuals. While the signalling role of avian plumage colour is relatively well studied, there has been much less research on coloration in avian bare parts. However, bare parts could be highly informative signals as they can show rapid changes in coloration. We measured bill colour (a ubiquitous bare part) in over 1600 passerine species and tested whether interspecific variation in carotenoid-based coloration is consistent with signalling to potential mates or signalling to potential rivals in a competitive context. Our results suggest that carotenoid bill coloration primarily evolved as a signal of dominance, as this type of coloration is more common in species that live in social groups in the non-breeding season, and species that nest in colonies; two socio-ecological conditions that promote frequent agonistic interactions with numerous and/or unfamiliar individuals. Additionally, our study suggests that carotenoid bill coloration is independent of the intensity of past sexual selection, as it is not related to either sexual dichromatism or sexual size dimorphism. These results pose a significant challenge to the conventional view that carotenoid-based avian coloration has evolved as a developmentally costly, condition-dependent sexual signal. We also suggest that bare part ornamentation may often signal different information than plumage ornaments.

Data from: Carotenoids and amphibians: effects on life history and susceptibility to the infectious pathogen, Batrachochytrium dendrobatidis

Carotenoids are considered beneficial nutrients because they provide increased immune capacity. Although carotenoid research has been conducted in many vertebrates, little research has been done in amphibians, a group that is experiencing global population declines from numerous causes, including disease. We raised two amphibian species through metamorphosis on three carotenoid diets to quantify the effects on life-history traits and post-metamorphic susceptibility to a fungal pathogen (Batrachochytrium dendrobatidis; Bd). Increased carotenoids had no effect on survival to metamorphosis in gray treefrogs (Hyla versicolor) but caused lower survival to metamorphosis in wood frogs [Lithobates sylvaticus (Rana sylvatica)]. Increased carotenoids caused both species to experience slower development and growth. When exposed to Bd after metamorphosis, wood frogs experienced high mortality, and the carotenoid diets had no mitigating effects. Gray treefrogs were less susceptible to Bd, which prevented an assessment of whether carotenoids could mitigate the effects of Bd. Moreover, carotenoids had no effect on pathogen load. As one of only a few studies examining the effects of carotenoids on amphibians and the first to examine potential interactions with Bd, our results suggest that carotenoids do not always serve amphibians in the many positive ways that have become the paradigm in other vertebrates.

Data from: Plasma carotenoid concentrations of incubating American kestrels (Falco sparverius) show annual, seasonal, and individual variation and explain reproductive outcome

In wild birds, the proximate and ultimate factors that affect circulating carotenoid concentrations remain poorly understood. We studied variation in plasma carotenoid concentrations across several scales: annual, seasonal, pair, territory and individual, and evaluated whether plasma carotenoid concentrations explained reproductive outcome of wild American kestrels (Falco sparverius). We sampled plasma carotenoid concentrations of 99 female and 80 male incubating kestrels from April to June in 2008 to 2012. Plasma carotenoid concentrations were explained by an interaction between year and sex, date, and random effects for pair and individual identity. In general, plasma carotenoid concentrations of males were significantly higher than females, but this depended on year. Within a breeding season, earlier nesting kestrels had higher carotenoid concentrations than later nesting kestrels, a pattern that is coincident with seasonal trends in local fitness. Pair and individual identity explained variation in carotenoid concentrations suggesting that carotenoid concentrations of mated birds were correlated, and some individuals consistently maintained higher carotenoid levels than others. Male carotenoid concentrations were positively associated with number of young fledged per pair. These results are consistent with the hypothesis that higher quality individuals have higher carotenoid levels compared to lower quality individuals, despite annual variations in carotenoid availability.