Matthew B Toomey

Washington University in St. Louis | WUSTL , Wash U · Department of Pathology and Immunology

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 un...

Carotenoid pigments underlie most of the red, orange, and yellow visual signals used in mate choice in vertebrates. However, many of the underlying processes surrounding the production of carotenoid-based traits remain unclear due to the complex nature of carotenoid uptake, metabolism, and deposition across tissues. Here, we leverage the ability to...

Red coloration is a salient feature of the natural world. Many vertebrates produce red color by converting dietary yellow carotenoids into red ketocarotenoids via an unknown mechanism. Here, we show that two enzymes, cytochrome P450 2J19 (CYP2J19) and 3-hydroxybutyrate dehydrogenase 1-like (BDH1L), are sufficient to catalyze this conversion. In bir...

Carotenoid pigments serve many endogenous functions in organisms, but some of the more fascinating are the external displays of carotenoids in the colorful red, orange and yellow plumages of birds. Since Darwin, biologists have been curious about the selective advantages (e.g., mate attraction) of having such ornate features, and, more recently, ad...

Animal pigment patterns play important roles in behavior and, in many species, red coloration serves as an honest signal of individual quality in mate choice. Among Danio fishes, some species develop erythrophores, pigment cells that contain red ketocarotenoids, whereas other species, like zebrafish (D. rerio) only have yellow xanthophores. Here, w...

Carotenoids color many of the red, orange and yellow ornaments of birds and also shape avian vision. The carotenoid-pigmented oil droplets in cone photoreceptors filter incoming light and are predicted to aid in color discrimination. Carotenoid use in both avian coloration and color vision raises an intriguing question: is the evolution of visual s...

Animal pigment patterns play important roles in behavior and, in many species, red coloration serves as an honest signal of individual quality in mate choice. Among Danio fishes, some species develop erythrophores, pigment cells that contain red ketocarotenoids, whereas other species, like zebrafish (D. rerio) only have yellow xanthophores. Here, w...

Canaries changing colors Many animals are sexually dimorphic, with different phenotypes in males and females. To identify the genetic basis of sexual differences in bird coloration, Gazda et al. investigated red coloration in mosaic canaries and related species (see the Perspective by Chen). Using a combination of genetic crosses, genomic mapping,...

Unlike wild and domestic canaries (Serinus canaria), or any of the three dozen species of finches in genus Serinus, the domestic urucum breed of canaries exhibits bright red bills and legs. This novel trait offers a unique opportunity to understand the mechanisms of bare-part coloration in birds. To identify the mutation producing the colorful phen...

A BSTRACT Unlike wild and domestic canaries ( Serinus canaria ), or any of the three dozen species of finches in genus Serinus , the domestic urucum breed of canaries exhibits bright red bills and legs. This novel bare-part coloration offers a unique opportunity to understand how leg and bill coloration evolve in birds. To identify the causative lo...

Thyroid hormone (TH) regulates diverse developmental events and can drive disparate cellular outcomes. In zebrafish, TH has opposite effects on neural crest derived pigment cells of the adult stripe pattern, limiting melanophore population expansion, yet increasing yellow/orange xanthophore numbers. To learn how TH elicits seemingly opposite respon...

Carotenoid-based coloration in birds is widely considered an honest signal of individual condition, but the mechanisms responsible for condition dependency in such ornaments remain debated. Currently, the most common explanation for how carotenoid coloration serves as a reliable signal of condition is the resource trade-off hypothesis, which propos...

Circulating endocrine factors are critical for orchestrating complex developmental processes during the generation of adult form. One such factor, thyroid hormone, regulates diverse cellular processes during post-embryonic development and can drive disparate morphological outcomes through mechanisms that remain essentially unknown. We sought to def...

Discrete colour morphs coexisting within a single population are common in nature. In a broad range of organisms, sympatric colour morphs often display major differences in other traits, including morphology, physiology or behaviour. Despite the repeated occurrence of this phenomenon, our understanding of the genetics that underlie multi-trait diff...

Urban environments create a unique suite of conditions, leading to changes in animal behavior, morphology, phenology, and physiology. Condition-dependent traits such as the carotenoid-based coloration offer a unique opportunity to assess the impacts of urbanization on organisms because they reflect the nutrition, health, or other resource-based att...

Dietary carotenoids have been proposed to boost immune system and antioxidant functions in vertebrate animals, but studies aimed at testing these physiological functions of carotenoids have often failed to find support. Here we subject yellow canaries (Serinus canaria), which possess high levels of carotenoids in their tissue, and white recessive c...

To distinguish colors, the nervous system must compare the activity of distinct subtypes of photoreceptors that are maximally sensitive to different portions of the light spectrum. In vertebrates, a variety of adaptations have arisen to refine the spectral sensitivity of cone photoreceptors and improve color vision. In this review article, we focus...

The spectral composition of ambient light varies across both space and time. Many species of jawed vertebrates adapt to this variation by tuning the sensitivity of their photoreceptors via the expression of CYP27C1, an enzyme that converts vitamin A1 into vitamin A2, thereby shifting the ratio of vitamin A1-based rhodopsin to red-shifted vitamin A2...

Significance The yellow, orange, and red colors of birds are produced through the deposition of carotenoid pigments into feathers and skin, and often function as signals in aggressive interactions and mate choice. These colors are hypothesized to communicate information about individual quality because their expression is linked to vital cellular p...

The retinae of many bird species contain a depression with high photoreceptor density known as the fovea. Many species of raptors have two foveae, a deep central fovea and a shallower temporal fovea. Birds have six types of photoreceptors: rods, active in dim light, double cones that are thought to mediate achromatic discrimination, and four types...

The PCR primers used in studies of enzyme function and expression. (a) PCR primers used to clone in situ hybridization templates. (b) Primers used for qPCR quantification of apocarotenoid-metabolizing enzyme transcript expression in developing chicken retinas. (c) PCR primers used to clone full-length transcripts of apocarotenoid-metabolizing enzym...

The number of discriminable colors predicted using the receptor noise-limited model with species-specific ocular media transmittance, spectral sensitivity measures, and varying positions of the C-type oil droplet filtering cutoff.The increment spectral sensitivity values calculated for the 11 UVS and 7 VS species with matched and mismatched C-type...

The species included in our phylogenetic comparison of retina apocarotenoid composition. The tuning of the SWS1 opsin is inferred from the amino acid at position 90 of the second transmembrane helix (Ödeen and Håstad, 2013; 2009). The amino acid sequence was either derived from previously published studies or was determined by sequencing of genomic...

The measured oil droplet spectra, pure carotenoid spectra, and model fit parameters for each measured C-type droplet.DOI: http://dx.doi.org/10.7554/eLife.15675.011

The species and visual system parameters used to model avian color discrimination. DOI: http://dx.doi.org/10.7554/eLife.15675.021

Apocarotenoid concentration and transcript expression levels for each biological and technical replicate.DOI: http://dx.doi.org/10.7554/eLife.15675.016

ELife digest The pioneering eye doctor André Rochon-Duvigneaud once wrote that “a bird is a wing guided by an eye”. With this statement, he underscored the sophistication of the bird’s eye, which surpasses our own in several respects. Compared to humans who have three types of cone photoreceptor, birds have four, meaning they can see an extra dimen...

The yellow and red feather pigmentation of many bird species [1] plays pivotal roles in social signaling and mate choice [2, 3]. To produce red pigments, birds ingest yellow carotenoids and endogenously convert them into red ketocarotenoids via an oxidation reaction catalyzed by a previously unknown ketolase [4-6]. We investigated the genetic basis...

In humans, a considerable fraction of the retinoid pool in skin is derived from vitamin A2 (all-trans 3,4-dehydroretinal). Vitamin A2 may be locally generated by keratinocytes, which can convert vitamin A1 (all-trans retinol) into vitamin A2 in cell culture. We report that human cytochrome P450 (hP450) 27C1, a previously 'orphan' enzyme, can cataly...

Diet-derived carotenoid pigments are concentrated in the retinas of birds and serve a variety of functions, including photoprotection. In domesticated bird species (e.g., chickens and quail), retinal carotenoid pigmentation has been shown to respond to large manipulations in light exposure and provide protection against photodamage. However, it is...

Some vertebrate species have evolved means of extending their visual sensitivity beyond the range of human vision. One mechanism of enhancing sensitivity to long-wavelength light is to replace the 11-cis retinal chromophore in photopigments with 11-cis 3,4-didehydroretinal. Despite over a century of research on this topic, the enzymatic basis of th...

Vision is the primary sensory modality of birds, and its importance is evident in the sophistication of their visual systems. Coloured oil droplets in the cone photoreceptors represent an adaptation in the avian retina, acting as long-pass colour filters. However, we currently lack understanding of how the optical properties and morphology of compo...

The brilliantly coloured cone oil droplets of the avian retina function as long-pass cut-off filters that tune the spectral sensitivity of the photoreceptors and are hypothesized to enhance colour discrimination and improve colour constancy. Although it has long been known that these droplets are pigmented with carotenoids, their precise compositio...

Worldwide urbanization continues to present new selection pressures on organisms. Carotenoid pigmentation of animals provides an ideal study system for identifying the source and significance of urban impacts because it is an environmentally derived trait and carotenoid molecules have widespread physiological, phenotypic, and fitness functions. Pri...

Carotenoids accumulate at high concentrations in the avian retina, where they filter incoming light, tune spectral sensitivity, and provide protection from damaging UV light. Among wild house finches (Haemorhous mexicanus), we have observed significant seasonal variation in retinal carotenoid levels, with a peak during the non‐reproductive winter p...

Carotenoid pigments are involved in different physiological processes (e.g., immunoenhancement, antioxidant activity) in addition to coloring plumage and integuments. As animals cannot synthesize these pigments de novo, it has been proposed that carotenoids constitute a limiting resource that birds may specifically seek in their food. Confirming th...

Many animals consume colorful foods, because bright coloration either enhances conspicuousness of food items or signals nutritional rewards. A comparatively under-studied aspect of food color preferences is the role of the background environment in shaping food detectability and choices. Previous work with house finches (Carpodacus mexicanus), for...

The coevolution of male traits and female mate preferences has led to the elaboration and diversification of sexually selected traits; however the mechanisms that mediate trait-preference coevolution are largely unknown. Carotenoid acquisition and accumulation are key determinants of the expression of male sexually selected carotenoid-based colorat...

Supplementary Data. Table S1 and figures S1 and S2 comparing the coloration of a sample of 75 wild male house finches and the experimentally manipulated stimulus males used in the mate choice trials.

Supplementary Methods. A detailed description of the parameters and calculations used to calculate avian visual contrasts and color-space parameters.

Images of experimental food and lighting conditions. (A) A sample image of the red food pellets and inedible gray paper distracters presented to the birds; (B) Unfiltered full-lighting conditions in our study room (left panel) compared to the red-filtered-lighting conditions (right panel). (DOC)

A detailed description of the methods used to measure the irradiance of the room lights and food and background spectral reflectance and the calculations of avian visual contrasts. (DOC)

For many bird species, vision is the primary sensory modality used to locate and assess food items. The health and spectral sensitivities of the avian visual system are influenced by diet-derived carotenoid pigments that accumulate in the retina. Among wild House Finches (Carpodacus mexicanus), we have found that retinal carotenoid accumulation var...

Consistent individual differences in behaviour are widespread in animals, but the proximate mechanisms driving these differences remain largely unresolved. Parasitism and immune challenges are hypothesized to shape the expression of animal personality traits, but few studies have examined the influence of neonatal immune status on the development o...

Plasma glucose (P(Glu)) concentrations in birds are 1.5-2 times higher than those of mammals of similar body mass. In mammals, sustained elevations of P(Glu) lead to oxidative stress and free radical-mediated scavenging of endogenous vasodilators (e.g., nitric oxide), contributing to elevated blood pressure. Despite the relatively high P(Glu) level...

For a variety of technical and conceptual reasons, biologists have come to use several different methods to quantify the colors of animals. However, the relative abilities of these different color-scoring procedures to capture variation in the actual color-generating mechanisms—pigment or structural composition of the integument—have never been tes...

Carotenoid pigments accumulate in the retinas of many animals, including humans, where they play an important role in visual health and performance. Recently, birds have emerged as a model system for studying the mechanisms and functions of carotenoid accumulation in the retina. However, these studies have been limited to a small number of domestic...

The glossy sheen of healthy hair is an ideal of human beauty; however, glossiness has never been quantified in the context of non-human animal signaling. Glossiness, the specular reflectance characteristic of polished surfaces, has the potential to act as a signal of quality because it depends upon material integrity and cleanliness. Here, we under...

The costs of developing, maintaining, and activating the immune system have been cited as an important force shaping life-history evolution in animals. Immunological defenses require energy, nutrients and time that might otherwise be devoted to other life-history traits like sexual displays or reproduction. Carotenoid pigments in animals provide a...

Food color can be indicative of specific nutrients, and thus discrimination based on color can be a valuable foraging behavior. Several bird and fish species with carotenoid-based body ornamentation show color preferences for presumably carotenoid-rich red and orange foods. However, little is known within species about whether or not individuals wi...

Carotenoid pigments produce the bright yellow to red ornamental colors of many animals, especially birds, and must ultimately be derived from the diet. However, they are also valuable for many physiological functions (e.g., antioxidants, immunostimulants, photoprotection, visual tuning, yolk nourishment to embryos), and as a result they are present...

Iridescent colours have been fascinating to humans throughout history; they are flashy, shimmering, dynamic, and examples surround us, from the commonly seen iridescent sheen of oily street puddles to the exotic, gaudy displays of birds-of-paradise featured in nature documentaries. Iridescent colours and the structures that produce them have unique...

Summary 1. Studies of visual ecology generally focus on the tuning of the eye to the spectral environment. However, the environment may also shape vision if the availability of nutrients or other extrinsic stressors impact eye structure or function. 2. Carotenoids are diet-derived pigments that accumulate in the retinas of birds, where they provide...

To investigate carotenoid content in the retina of Japanese quail (Coturnix japonica), for comparison with carotenoids in human retina, and to assess the effects of different saponification procedures on the recovery of quail retinal carotenoids. Extracted retinal carotenoids were saponified with methods adapted from recent studies, then identified...

Florida scrub-jays are cooperative breeders that live in family groups consisting of a breeding pair, often with several non-breeding helpers. Florida scrub-jays cache food by scatter-hoarding items for later consumption. Within family groups, members have the opportunity to observe and pilfer the caches of other members. We observed jays harvestin...

Adult zebra mussels are generally thought of as sessile animals. However, when detached from their byssus, adult mussels exhibit creeping behavior similar to that of other bivalve species. Our study examined the effects of size, light, water hardness, temperature, and the presence of injured conspecifics on the movement of adult zebra mussels. Muss...