56 results on '"Matthew B. Toomey"'
Search Results
2. Evolution, Development and Function of Vertebrate Cone Oil Droplets
- Author
-
Matthew B. Toomey and Joseph C. Corbo
- Subjects
color vision ,spectral sensitivity ,carotenoids ,visual ecology ,photoprotection ,cone photoreceptor ,Neurosciences. Biological psychiatry. Neuropsychiatry ,RC321-571 - Abstract
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 on one such adaptation, the oil droplet, a unique optical organelle found within the inner segment of cone photoreceptors of a diverse array of vertebrate species, from fish to mammals. These droplets, which consist of neutral lipids and carotenoid pigments, are interposed in the path of light through the photoreceptor and modify the intensity and spectrum of light reaching the photosensitive outer segment. In the course of evolution, the optical function of oil droplets has been fine-tuned through changes in carotenoid content. Species active in dim light reduce or eliminate carotenoids to enhance sensitivity, whereas species active in bright light precisely modulate carotenoid double bond conjugation and concentration among cone subtypes to optimize color discrimination and color constancy. Cone oil droplets have sparked the curiosity of vision scientists for more than a century. Accordingly, we begin by briefly reviewing the history of research on oil droplets. We then discuss what is known about the developmental origins of oil droplets. Next, we describe recent advances in understanding the function of oil droplets based on biochemical and optical analyses. Finally, we survey the occurrence and properties of oil droplets across the diversity of vertebrate species and discuss what these patterns indicate about the evolutionary history and function of this intriguing organelle.
- Published
- 2017
- Full Text
- View/download PDF
3. Cambrian origin of the CYP27C1-mediated vitamin A1-to-A2 switch, a key mechanism of vertebrate sensory plasticity
- Author
-
Ala Morshedian, Matthew B. Toomey, Gabriel E. Pollock, Rikard Frederiksen, Jennifer M. Enright, Stephen D. McCormick, M. Carter Cornwall, Gordon L. Fain, and Joseph C. Corbo
- Subjects
visual ecology ,photoreceptor ,petromyzon marinus ,Science - Abstract
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-based porphyropsin in the eye. Here, we show that the sea lamprey (Petromyzon marinus), a jawless vertebrate that diverged from jawed vertebrates during the Cambrian period (approx. 500 Ma), dynamically shifts its photoreceptor spectral sensitivity via vitamin A1-to-A2 chromophore exchange as it transitions between photically divergent aquatic habitats. We further show that this shift correlates with high-level expression of the lamprey orthologue of CYP27C1, specifically in the retinal pigment epithelium as in jawed vertebrates. Our results suggest that the CYP27C1-mediated vitamin A1-to-A2 switch is an evolutionarily ancient mechanism of sensory plasticity that appeared not long after the origin of vertebrates.
- Published
- 2017
- Full Text
- View/download PDF
4. Development and genetics of red coloration in the zebrafish relative Danio albolineatus
- Author
-
Delai Huang, Victor M Lewis, Tarah N Foster, Matthew B Toomey, Joseph C Corbo, and David M Parichy
- Subjects
pigmentation ,Danio ,color pattern ,erythrophore ,carotenoid ,Medicine ,Science ,Biology (General) ,QH301-705.5 - Abstract
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, we use pearl danio (D. albolineatus) to assess the developmental origin of erythrophores and their mechanisms of differentiation. We show that erythrophores in the fin of D. albolineatus share a common progenitor with xanthophores and maintain plasticity in cell fate even after differentiation. We further identify the predominant ketocarotenoids that confer red coloration to erythrophores and use reverse genetics to pinpoint genes required for the differentiation and maintenance of these cells. Our analyses are a first step toward defining the mechanisms underlying the development of erythrophore-mediated red coloration in Danio and reveal striking parallels with the mechanism of red coloration in birds.
- Published
- 2021
- Full Text
- View/download PDF
5. The description of Haematococcus privus sp. nov. (Chlorophyceae, Chlamydomonadales) from North America
- Author
-
Mark A. Buchheim, Ashley Silver, Haley Johnson, Richard Portman, and Matthew B. Toomey
- Subjects
Plant Science ,Aquatic Science ,Ecology, Evolution, Behavior and Systematics - Abstract
An enormous body of research is focused on finding ways to commercialize carotenoids produced by the unicellular green alga, Haematococcus, often without the benefit of a sound phylogenetic assessment. Evidence of cryptic diversity in the genus means that comparing results of pigment studies may be confounded by the absence of a phylogenetic framework. Moreover, previous work has identified unnamed strains that are likely candidates for species status. We reconstructed the phylogeny of an expanded sampling of Haematococcus isolates utilizing data from nuclear ribosomal markers (18S rRNA gene, 26S rRNA gene, internal transcribed spacer [ITS]-1, 5.8S rRNA gene, and ITS-2) and the rbcL gene. In addition, we gathered morphological, ultrastructural and pigment data from key isolates of Haematococcus. Our expanded data and taxon sampling support the concept of a new species, H. privus, found exclusively in North America. Despite overlap in numerous morphological traits, results indicate that ratios of protoplast length to width and akinete diameter may be useful for discriminating Haematococcus lineages. High growth rate and robust astaxanthin yield indicate that H. rubicundus (SAG 34-1c) is worthy of additional scrutiny as a pigment source. With the description of H. privus, the evidence supports the existence of at least five, species-level lineages in the genus. Our phylogenetic assessment provides the tools to frame future pigment investigations of Haematococcus in an updated evolutionary context. In addition, our investigation highlighted open questions regarding polyploidy and sexuality in Haematococcus which demonstrate that much remains to be discovered about this green flagellate.
- Published
- 2023
6. Thyroid hormone regulates distinct paths to maturation in pigment cell lineages
- Author
-
Lauren M Saunders, Abhishek K Mishra, Andrew J Aman, Victor M Lewis, Matthew B Toomey, Jonathan S Packer, Xiaojie Qiu, Jose L McFaline-Figueroa, Joseph C Corbo, Cole Trapnell, and David M Parichy
- Subjects
pigmentation ,neural crest ,thyroid hormone ,post-embryonic development ,melanophore ,xanthophore ,Medicine ,Science ,Biology (General) ,QH301-705.5 - Abstract
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 responses in cells having a common embryological origin, we analyzed individual transcriptomes from thousands of neural crest-derived cells, reconstructed developmental trajectories, identified pigment cell-lineage specific responses to TH, and assessed roles for TH receptors. We show that TH promotes maturation of both cell types but in distinct ways. In melanophores, TH drives terminal differentiation, limiting final cell numbers. In xanthophores, TH promotes accumulation of orange carotenoids, making the cells visible. TH receptors act primarily to repress these programs when TH is limiting. Our findings show how a single endocrine factor integrates very different cellular activities during the generation of adult form.
- Published
- 2019
- Full Text
- View/download PDF
7. Testosterone Coordinates Gene Expression Across Different Tissues to Produce Carotenoid-Based Red Ornamentation
- Author
-
Sarah Khalil, Erik D Enbody, Carolina Frankl-Vilches, Joseph F Welklin, Rebecca E Koch, Matthew B Toomey, Simon Yung Wa Sin, Scott V Edwards, Manfred Gahr, Hubert Schwabl, Michael S Webster, and Jordan Karubian
- Subjects
Genetics ,Molecular Biology ,Ecology, Evolution, Behavior and Systematics - Abstract
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 experimentally induce the production of a carotenoid-based red plumage patch in the red-backed fairywren (Malurus melanocephalus), a songbird in which red plumage is an important male sexual signal. We experimentally elevated testosterone in unornamented males lacking red plumage to induce the production of ornamentation and compared gene expression in both the liver and feather follicles between unornamented control males, testosterone-implanted males, and naturally ornamented males. We show that testosterone upregulates the expression of CYP2J19, a gene known to be involved in ketocarotenoid metabolism, and a putative carotenoid processing gene (ELOVL6) in the liver, and also regulates the expression of putative carotenoid transporter genes in red feather follicles on the back, including ABCG1. In black feathers, carotenoid-related genes are downregulated and melanin genes upregulated, but we find that carotenoids are still present in the feathers. This may be due to the activity of the carotenoid-cleaving enzyme BCO2 in black feathers. Our study provides a first working model of a pathway for carotenoid-based trait production in free-living birds, implicates testosterone as a key regulator of carotenoid-associated gene expression, and suggests hormones may coordinate the many processes that underlie the production of these traits across multiple tissues.
- Published
- 2023
8. Methods for extracting and analyzing carotenoids from bird feathers
- Author
-
Matthew B, Toomey, Dustin J, Smith, Desirae M, Gonzales, and Kevin J, McGraw
- Subjects
Birds ,Pigmentation ,Animals ,Feathers ,Carotenoids ,Chromatography, High Pressure Liquid - Abstract
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, advances in biochemical methods have permitted researchers to explore the composition and characteristics of carotenoid pigments in feathers. Here we review contemporary methods for extracting and analyzing carotenoids in bird feathers, with special attention to the difficulties of removal from the feather keratin matrix, the possibility of feather carotenoid esterification and the strengths and challenges of different analytical methods like high-performance liquid chromatography and Raman spectroscopy. We also add an experimental test of current common extraction methods (e.g., mechanical, thermochemical) and find significant differences in the recovery of specific classes of carotenoids, suggesting that no single approach is best for all pigment or feather types.
- Published
- 2022
9. A mechanism for red coloration in vertebrates
- Author
-
Matthew B. Toomey, Cristiana I. Marques, Pedro M. Araújo, Delai Huang, Siqiong Zhong, Yu Liu, Gretchen D. Schreiner, Connie A. Myers, Paulo Pereira, Sandra Afonso, Pedro Andrade, Małgorzata A. Gazda, Ricardo J. Lopes, Ivan Viegas, Rebecca E. Koch, Maureen E. Haynes, Dustin J. Smith, Yohey Ogawa, Daniel Murphy, Rachel E. Kopec, David M. Parichy, Miguel Carneiro, and Joseph C. Corbo
- Subjects
Birds ,Hydroxybutyrate Dehydrogenase ,Cytochrome P-450 Enzyme System ,Pigmentation ,Animals ,Feathers ,General Agricultural and Biological Sciences ,Carotenoids ,General Biochemistry, Genetics and Molecular Biology - Abstract
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 birds, both enzymes are expressed at the sites of ketocarotenoid biosynthesis (feather follicles and red cone photoreceptors), and genetic evidence implicates these enzymes in yellow/red color variation in feathers. In fish, the homologs of CYP2J19 and BDH1L are required for ketocarotenoid production, and we show that these enzymes are sufficient to produce ketocarotenoids in cell culture and when ectopically expressed in fish skin. Finally, we demonstrate that the red-cone-enriched tetratricopeptide repeat protein 39B (TTC39B) enhances ketocarotenoid production when co-expressed with CYP2J19 and BDH1L. The discovery of this mechanism of ketocarotenoid biosynthesis has major implications for understanding the evolution of color diversity in vertebrates.
- Published
- 2022
10. Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds
- Author
-
Matthew B Toomey, Olle Lind, Rikard Frederiksen, Robert W Curley Jr, Ken M Riedl, David Wilby, Steven J Schwartz, Christopher C Witt, Earl H Harrison, Nicholas W Roberts, Misha Vorobyev, Kevin J McGraw, M Carter Cornwall, Almut Kelber, and Joseph C Corbo
- Subjects
spectral tuning ,carotenoids ,sensory ecology ,birds ,retina ,photoreceptors ,Medicine ,Science ,Biology (General) ,QH301-705.5 - Abstract
Color vision in birds is mediated by four types of cone photoreceptors whose maximal sensitivities (λmax) are evenly spaced across the light spectrum. In the course of avian evolution, the λmax of the most shortwave-sensitive cone, SWS1, has switched between violet (λmax > 400 nm) and ultraviolet (λmax < 380 nm) multiple times. This shift of the SWS1 opsin is accompanied by a corresponding short-wavelength shift in the spectrally adjacent SWS2 cone. Here, we show that SWS2 cone spectral tuning is mediated by modulating the ratio of two apocarotenoids, galloxanthin and 11’,12’-dihydrogalloxanthin, which act as intracellular spectral filters in this cell type. We propose an enzymatic pathway that mediates the differential production of these apocarotenoids in the avian retina, and we use color vision modeling to demonstrate how correlated evolution of spectral tuning is necessary to achieve even sampling of the light spectrum and thereby maintain near-optimal color discrimination.
- Published
- 2016
- Full Text
- View/download PDF
11. Author response: Development and genetics of red coloration in the zebrafish relative Danio albolineatus
- Author
-
Victor M Lewis, Matthew B. Toomey, Joseph C. Corbo, David M. Parichy, Delai Huang, and Tarah N Foster
- Subjects
Genetics ,biology ,Danio ,biology.organism_classification ,Zebrafish - Published
- 2021
12. Avian color expression and perception: is there a carotenoid link?
- Author
-
Matthew B. Toomey and Kelly L. Ronald
- Subjects
0106 biological sciences ,Visual perception ,genetic structures ,Physiology ,Color vision ,media_common.quotation_subject ,Color ,macromolecular substances ,Aquatic Science ,Biology ,010603 evolutionary biology ,01 natural sciences ,Birds ,03 medical and health sciences ,Perception ,Animals ,Molecular Biology ,Carotenoid ,Ecology, Evolution, Behavior and Systematics ,030304 developmental biology ,media_common ,chemistry.chemical_classification ,0303 health sciences ,Color Vision ,Pigmentation ,organic chemicals ,food and beverages ,Ornaments ,Feathers ,Carotenoids ,chemistry ,Expression (architecture) ,Evolutionary biology ,Plumage ,Insect Science ,Oil droplet ,Animal Science and Zoology ,sense organs - Abstract
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 signals and signal perception linked through these pigments? Here, we explore the genetic, physiological and functional connections between these traits. Carotenoid color and droplet pigmentation share common mechanisms of metabolic conversion and are both affected by diet and immune system challenges. Yet, the time scale and magnitude of these effects differ greatly between plumage and the visual system. Recent observations suggest a link between retinal carotenoid levels and color discrimination performance, but the mechanisms underlying these associations remain unclear. Therefore, we performed a modeling exercise to ask whether and how changes in droplet carotenoid content could alter the perception of carotenoid-based plumage. This exercise revealed that changing oil droplet carotenoid concentration does not substantially affect the discrimination of carotenoid-based colors, but might change how reliably a receiver can predict the carotenoid content of an ornament. These findings suggest that, if present, a carotenoid link between signal and perception is subtle. Deconstructing this relationship will require a deeper understanding of avian visual perception and the mechanisms of color production. We highlight several areas where we see opportunities to gain new insights, including comparative genomic studies of shared mechanisms of carotenoid processing and alternative approaches to investigating color vision.
- Published
- 2021
13. Development and genetics of red coloration in the zebrafish relativeDanio albolineatus
- Author
-
Victor M Lewis, Joseph C. Corbo, Delai Huang, David M. Parichy, and Matthew B. Toomey
- Subjects
biology ,Mate choice ,Evolutionary biology ,Danio ,Pigment cells ,biology.organism_classification ,Zebrafish - Abstract
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. AmongDaniofishes, some species develop erythrophores, pigment cells that contain red ketocarotenoids, whereas other species, like zebrafish (D. rerio) only have yellow xanthophores. Here, we use pearl danio (D. albolineatus) to assess the developmental origin of erythrophores and their mechanisms of differentiation. We show that erythrophores in the fin ofD. albolineatusshare a common progenitor with xanthophores and maintain plasticity in cell fate even after differentiation. We further identify the predominant ketocarotenoids that confer red coloration to erythrophores and use reverse genetics to pinpoint genes required for the differentiation and maintenance of these cells. Our analyses are a first step towards defining the mechanisms underlying the development of erythrophore-mediated red coloration inDanioand reveal striking parallels with the mechanism of red coloration in birds.
- Published
- 2021
14. Genetic Basis of De Novo Appearance of Carotenoid Ornamentation in Bare Parts of Canaries
- Author
-
Miguel Carneiro, Matthew B. Toomey, Philip D. Kiser, Pedro Araújo, Connie A. Myers, Sandra Afonso, Małgorzata Anna Gazda, Joseph C. Corbo, Geoffrey E. Hill, Kyla Serres, and Ricardo Lopes
- Subjects
0106 biological sciences ,Canaries ,Zoology ,Genes, Recessive ,010603 evolutionary biology ,01 natural sciences ,Genome ,Mixed Function Oxygenases ,03 medical and health sciences ,Gene mapping ,biology.animal ,Genetics ,Missense mutation ,Animals ,Molecular Biology ,Gene ,Carotenoid ,Ecology, Evolution, Behavior and Systematics ,030304 developmental biology ,chemistry.chemical_classification ,0303 health sciences ,biology ,Pigmentation ,Phenotype ,Carotenoids ,Breed ,chemistry ,Amino Acid Substitution ,Serinus canaria - Abstract
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 phenotype, we resequenced the genome of urucum canaries and performed a range of analyses to search for genotype-to-phenotype associations across the genome. We identified a nonsynonymous mutation in the gene BCO2 (beta-carotene oxygenase 2, also known as BCDO2), an enzyme involved in the cleavage and breakdown of full-length carotenoids into short apocarotenoids. Protein structural models and in vitro functional assays indicate that the urucum mutation abrogates the carotenoid-cleavage activity of BCO2. Consistent with the predicted loss of carotenoid-cleavage activity, urucum canaries tended to have increased levels of full-length carotenoid pigments in bill tissue and reduced levels of carotenoid-cleavage products (apocarotenoids) in retinal tissue compared with other breeds of canaries. We hypothesize that carotenoid-based bare-part coloration might be readily gained, modified, or lost through simple switches in the enzymatic activity or regulation of BCO2 and this gene may be an important mediator in the evolution of bare-part coloration among bird species.
- Published
- 2020
15. No evidence that carotenoid pigments boost either immune or antioxidant defenses in a songbird
- Author
-
Yufeng Zhang, Rebecca E. Koch, Dennis Hasselquist, Andreas N. Kavazis, Geoffrey E. Hill, Matthew B. Toomey, and Wendy R. Hood
- Subjects
Lipopolysaccharides ,0106 biological sciences ,0301 basic medicine ,Canaries ,Antioxidant ,medicine.drug_class ,medicine.medical_treatment ,Science ,General Physics and Astronomy ,Zoology ,macromolecular substances ,medicine.disease_cause ,010603 evolutionary biology ,01 natural sciences ,Antioxidants ,Article ,General Biochemistry, Genetics and Molecular Biology ,03 medical and health sciences ,Immune system ,Tetanus Toxoid ,medicine ,polycyclic compounds ,Animals ,Retinoid ,lcsh:Science ,Carotenoid ,chemistry.chemical_classification ,Gene knockdown ,Multidisciplinary ,biology ,Pigmentation ,organic chemicals ,food and beverages ,Pigments, Biological ,General Chemistry ,Scavenger Receptors, Class B ,biology.organism_classification ,Carotenoids ,Immunity, Innate ,biological factors ,Songbird ,White (mutation) ,030104 developmental biology ,Gene Expression Regulation ,chemistry ,Mutation ,lcsh:Q ,Oxidative stress - Abstract
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 canaries, which possess a knockdown mutation that results in very low levels of tissue carotenoids, to oxidative and pathogen challenges. Across diverse measures of physiological performance, we detect no differences between carotenoid-rich yellow and carotenoid-deficient white canaries. These results add further challenge to the assumption that carotenoids are directly involved in supporting physiological function in vertebrate animals. While some dietary carotenoids provide indirect benefits as retinoid precursors, our observations suggest that carotenoids themselves may play little to no direct role in key physiological processes in birds., Dietary carotenoids have been proposed to have physiological benefits in addition to contributing to coloration. Here, Koch et al. compare immune and antioxidant functions in yellow, carotenoid-rich vs. white, carotenoid-deficient canaries and find no difference, suggesting a limited physiological role of carotenoids.
- Published
- 2018
16. The effects of dietary carotenoid supplementation and retinal carotenoid accumulation on vision-mediated foraging in the house finch.
- Author
-
Matthew B Toomey and Kevin J McGraw
- Subjects
Medicine ,Science - Abstract
BACKGROUND: 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 varies significantly among individuals and is related to dietary carotenoid intake. If diet-induced changes in retinal carotenoid accumulation alter spectral sensitivity, then they have the potential to affect visually mediated foraging performance. METHODOLOGY/PRINCIPAL FINDINGS: In two experiments, we measured foraging performance of house finches with dietarily manipulated retinal carotenoid levels. We tested each bird's ability to extract visually contrasting food items from a matrix of inedible distracters under high-contrast (full) and dimmer low-contrast (red-filtered) lighting conditions. In experiment one, zeaxanthin-supplemented birds had significantly increased retinal carotenoid levels, but declined in foraging performance in the high-contrast condition relative to astaxanthin-supplemented birds that showed no change in retinal carotenoid accumulation. In experiments one and two combined, we found that retinal carotenoid concentrations predicted relative foraging performance in the low- vs. high-contrast light conditions in a curvilinear pattern. Performance was positively correlated with retinal carotenoid accumulation among birds with low to medium levels of accumulation (∼0.5-1.5 µg/retina), but declined among birds with very high levels (>2.0 µg/retina). CONCLUSION/SIGNIFICANCE: Our results suggest that carotenoid-mediated spectral filtering enhances color discrimination, but that this improvement is traded off against a reduction in sensitivity that can compromise visual discrimination. Thus, retinal carotenoid levels may be optimized to meet the visual demands of specific behavioral tasks and light environments.
- Published
- 2011
- Full Text
- View/download PDF
17. Specialized photoreceptor composition in the raptor fovea
- Author
-
Matthew B. Toomey, Joseph C. Corbo, Mindaugas Mitkus, Peter Olsson, and Almut Kelber
- Subjects
Male ,0301 basic medicine ,Fovea Centralis ,Rhodopsin ,Opsin ,Eurasian sparrowhawk ,genetic structures ,Color vision ,Color ,Zoology ,Milvus milvus ,Article ,Retina ,03 medical and health sciences ,0302 clinical medicine ,Microscopy, Electron, Transmission ,Species Specificity ,Retinal Rod Photoreceptor Cells ,biology.animal ,medicine ,Animals ,Opsins ,Raptors ,biology ,General Neuroscience ,Anatomy ,Buteo buteo ,biology.organism_classification ,eye diseases ,Buzzard ,030104 developmental biology ,medicine.anatomical_structure ,Pernis apivorus ,Retinal Cone Photoreceptor Cells ,Female ,sense organs ,030217 neurology & neurosurgery - Abstract
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 of single cones mediating color vision. To maximize visual acuity, the fovea should only contain photoreceptors contributing to high-resolution vision. Interestingly, it has been suggested that raptors might lack double cones in the fovea. We used transmission electron microscopy and immunohistochemistry to evaluate this claim in five raptor species: the common buzzard (Buteo buteo), the honey buzzard (Pernis apivorus), the Eurasian sparrowhawk (Accipiter nisus), the red kite (Milvus milvus), and the peregrine falcon (Falco peregrinus). We found that all species, except the Eurasian sparrowhawk, lack double cones in the center of the central fovea. The size of the double cone-free zone differed between species. Only the common buzzard had a double cone-free zone in the temporal fovea. In three species, we examined opsin expression in the central fovea and found evidence that rod opsin positive cells were absent and violet-sensitive cone and green-sensitive cone opsin positive cells were present. We conclude that not only double cones, but also single cones may contribute to high-resolution vision in birds, and that raptors may in fact possess high-resolution tetrachromatic vision in the central fovea.
- Published
- 2017
18. Genetic Basis ofDe NovoAppearance of Carotenoid Ornamentation in Bare-Parts of Canaries
- Author
-
Pedro Araújo, Sandra Afonso, Matthew B. Toomey, Philip D. Kiser, Geoffrey E. Hill, Miguel Carneiro, Małgorzata Anna Gazda, Ricardo Lopes, Connie A. Myers, Joseph C. Corbo, and Kyla Serres
- Subjects
chemistry.chemical_classification ,Genetics ,Oxygenase ,biology ,Locus (genetics) ,Genome ,Pigment ,chemistry ,biology.animal ,visual_art ,visual_art.visual_art_medium ,Missense mutation ,Gene ,Carotenoid ,Serinus canaria - Abstract
Unlike wild and domestic canaries (Serinus canaria), or any of the three dozen species of finches in genusSerinus, 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 locus, we resequenced the genome of urucum canaries and performed a range of analyses to search for genotype-to-phenotype associations across the genome. We identified a nonsynonymous mutation in the geneBCO2(beta-carotene oxygenase 2, also known asBCDO2), an enzyme involved in the cleavage and breakdown of full-length carotenoids into short apocarotenoids. Protein structural models andin vitrofunctional assays indicate that the urucum mutation abrogates the carotenoid cleavage activity of BCO2. Consistent with the predicted loss of carotenoid cleavage activity, urucum canaries had increased levels of full-length carotenoid pigments in bill tissue and a significant reduction in levels of carotenoid cleavage products (apocarotenoids) in retinal tissue compared to other breeds of canaries. We hypothesize that carotenoid-based bare-part coloration might be readily gained, modified, or lost through simple switches in the enzymatic activity or regulation ofBCO2and this gene may be an important mediator in the evolution of bare-part coloration among bird species.
- Published
- 2019
19. Author response: Thyroid hormone regulates distinct paths to maturation in pigment cell lineages
- Author
-
Lauren M. Saunders, Cole Trapnell, Matthew B. Toomey, David M. Parichy, Victor M Lewis, Joseph C. Corbo, Andy Aman, Xiaojie Qiu, Abhishek Kumar Mishra, Jonathan S. Packer, and José L. McFaline-Figueroa
- Subjects
Pigment ,medicine.anatomical_structure ,visual_art ,Cell ,Thyroid ,medicine ,visual_art.visual_art_medium ,Biology ,Cell biology ,Hormone - Published
- 2019
20. Testing the resource tradeoff hypothesis for carotenoid-based signal honesty using genetic variants of the domestic canary
- Author
-
Andreas N. Kavazis, Matthew B. Toomey, Geofsfrey E. Hill, Rebecca E. Koch, Dennis Hasselquist, and Molly Staley
- Subjects
Male ,Canaries ,Future studies ,Resource (biology) ,Physiology ,media_common.quotation_subject ,Color ,Zoology ,Aquatic Science ,Trade-off ,Antioxidants ,biology.animal ,Honesty ,Animals ,Molecular Biology ,Carotenoid ,Ecology, Evolution, Behavior and Systematics ,media_common ,chemistry.chemical_classification ,biology ,Pigmentation ,Genetic variants ,Ornaments ,Feathers ,Carotenoids ,Immunity, Innate ,Animal Communication ,chemistry ,Insect Science ,Female ,Animal Science and Zoology ,Cues ,Serinus canaria - Abstract
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 proposes that use of carotenoids for ornaments reduces their availability for use by the immune system or for protection from oxidative damage. However, two main assumptions of the hypothesis remain in question: whether carotenoids boost the performance of internal processes such as immune and antioxidant defenses, and whether allocating carotenoids to ornaments imposes a trade-off with such benefits. In this study, we tested these two fundamental assumptions using types of domestic canary (Serinus canaria domestica) that enable experiments in which carotenoid availability and allocation can be tightly controlled. Specifically, we assessed metrics of immune and antioxidant performance in three genetic variants of the color-bred canary that differ only in carotenoid phenotype: ornamented, carotenoid-rich yellow canaries; unornamented, carotenoid-rich 'white dominant' canaries; and unornamented, carotenoid-deficient 'white recessive' canaries. The resource trade-off hypothesis predicts that carotenoid-rich individuals should outperform carotenoid-deficient individuals and that birds that allocate carotenoids to feathers should pay a cost in the form of reduced immune function or greater oxidative stress compared with unornamented birds. We found no evidence to support either prediction; all three canary types performed equally across measures. We suggest that testing alternative mechanisms for the honesty of carotenoid-based coloration should be a key focus of future studies of carotenoid-based signaling in birds.
- Published
- 2019
21. Human cytochrome P450 27C1 catalyzes 3,4‐desaturation of retinoids
- Author
-
Yi Xiao, Joseph C. Corbo, Jennifer M. Enright, Thanh T.N. Phan, F. P. Guengerich, Matthew B. Toomey, Leslie D. Nagy, Kevin M. Johnson, Valerie M. Kramlinger, and Rina Fujiwara
- Subjects
0301 basic medicine ,medicine.drug_class ,Biophysics ,Retinoic acid ,Biochemistry ,Article ,law.invention ,Retinoids ,03 medical and health sciences ,chemistry.chemical_compound ,food ,Structural Biology ,law ,Genetics ,medicine ,Humans ,Cytochrome P450 Family 27 ,Retinoid ,Molecular Biology ,Vitamin a1 ,chemistry.chemical_classification ,030102 biochemistry & molecular biology ,biology ,Retinol ,Cytochrome P450 ,Retinal ,Cell Biology ,030104 developmental biology ,Enzyme ,chemistry ,biology.protein ,Recombinant DNA ,food.nutrient - Abstract
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 catalyze this reaction. Purified recombinant hP450 27C1 bound and desaturated all-trans retinol, retinal, and retinoic acid, as well as 11-cis-retinal. Although the physiological role of 3,4-dehydroretinoids in humans is unclear, we have identified hP450 27C1 as an enzyme capable of efficiently mediating their formation.
- Published
- 2016
22. Cyp27c1 Red-Shifts the Spectral Sensitivity of Photoreceptors by Converting Vitamin A1 into A2
- Author
-
Nicholas W. Roberts, Rina Fujiwara, Leslie D. Nagy, Matthew B. Toomey, Joseph C. Corbo, Vladimir J. Kefalov, Shelby E. Temple, James R. Allen, Yi Xiao, F. Peter Guengerich, Shinya Sato, Stephen L. Johnson, Kevin M. Johnson, Jennifer M. Enright, Martin J. How, and Valerie M. Kramlinger
- Subjects
Infrared Rays ,General Biochemistry, Genetics and Molecular Biology ,Amphibian Proteins ,chemistry.chemical_compound ,food ,Cytochrome P-450 Enzyme System ,Animals ,Photopigment ,Vitamin A ,Zebrafish ,Retinal chromophore ,Vitamin a1 ,Rana catesbeiana ,biology ,Agricultural and Biological Sciences(all) ,Biochemistry, Genetics and Molecular Biology(all) ,Retinal ,Zebrafish Proteins ,biology.organism_classification ,Cell biology ,Cytochrome P450 Family ,Spectral sensitivity ,Biochemistry ,chemistry ,Visual Perception ,food.nutrient ,General Agricultural and Biological Sciences ,Vitamin A2 ,Transcriptome ,Photoreceptor Cells, Vertebrate - Abstract
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 this perceptual switch remains unknown. Here, we show that a cytochrome P450 family member, Cyp27c1, mediates this switch by converting vitamin A1 (the precursor of 11-cis retinal) into vitamin A2 (the precursor of 11-cis 3,4-didehydroretinal). Knockout of cyp27c1 in zebrafish abrogates production of vitamin A2, eliminating the animal's ability to red-shift its photoreceptor spectral sensitivity and reducing its ability to see and respond to near-infrared light. Thus, the expression of a single enzyme mediates dynamic spectral tuning of the entire visual system by controlling the balance of vitamin A1 and A2 in the eye.
- Published
- 2015
- Full Text
- View/download PDF
23. Expression of and choice for condition-dependent carotenoid-based color in an urbanizing context
- Author
-
Pierce Hutton, Kevin J. McGraw, Matthew B. Toomey, Mathieu Giraudeau, School of Life Sciences [Tempe, USA], Arizona State University [Tempe] (ASU), University of Exeter, Washington University School of Medicine in St. Louis, and Washington University in Saint Louis (WUSTL)
- Subjects
0106 biological sciences ,0301 basic medicine ,urbanization ,genetic structures ,[SDV]Life Sciences [q-bio] ,Zoology ,Context (language use) ,Biology ,coloration ,010603 evolutionary biology ,01 natural sciences ,03 medical and health sciences ,Urbanization ,mate choice ,Carotenoid ,Ecology, Evolution, Behavior and Systematics ,chemistry.chemical_classification ,Phenology ,condition-dependent traits ,030104 developmental biology ,Habitat ,chemistry ,Mate choice ,Plumage ,Color preferences ,Animal Science and Zoology - Abstract
International audience; 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 attributes of their bearers and they play an essential role in intra and intersex interactions. To determine if and how the carotenoid-based coloration of male house finches (Haemorhous mexicanus) varies along a gradient of urbanization, we quantified the plumage coloration of more than 1000 individuals in urban, suburban, rural, and desert habitats over the course of 17 months. We also examined for the first time the preference of females for male plumage coloration across the urban-rural gradient, to test if and how female preferences varied relative to the plumage coloration displayed by males in their local population. We found that carotenoid-based coloration decreased along the gradient of urbanization, suggesting that the enzyme-driven metabolic conversion of dietary carotenoids into red carotenoids used to color plumage is sensitive to urban stressors. The stronger negative effect of urbanization on carotenoid-based plumage coloration during breeding than during molt and winter suggests that urbanization affects color fading rate, maybe through modifications of feather-degrading bacterial load. Finally, we have shown that urbanization influences female mate-choice behavior, suggesting that female color preferences may track the variation in male coloration across the gradient of urbanization.
- Published
- 2018
24. A non-coding region near
- Author
-
Matthew B, Toomey, Cristiana I, Marques, Pedro, Andrade, Pedro M, Araújo, Stephen, Sabatino, Małgorzata A, Gazda, Sandra, Afonso, Ricardo J, Lopes, Joseph C, Corbo, and Miguel, Carneiro
- Subjects
Avian Proteins ,Songbirds ,Follistatin ,Polymorphism, Genetic ,Sex Chromosomes ,Pigmentation ,Sequence Analysis, RNA ,Animals ,Color ,Genetics and Genomics ,Finches - Abstract
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 differences and the factors that promote the long-term maintenance of phenotypic variability within a freely interbreeding population are incomplete. Here, we investigated the genetic basis of red and black head colour in the Gouldian finch (Erythrura gouldiae), a classic polymorphic system in which naturally occurring colour morphs also display differences in aggressivity and reproductive success. We show that the candidate locus is a small (approx. 70 kb) non-coding region mapping to the Z chromosome near the Follistatin (FST) gene. Unlike recent findings in other systems where phenotypic morphs are explained by large inversions containing hundreds of genes (so-called supergenes), we did not identify any structural rearrangements between the two haplotypes using linked-read sequencing technology. Nucleotide divergence between the red and black alleles was high when compared to the remainder of the Z chromosome, consistent with their maintenance as balanced polymorphisms over several million years. Our results illustrate how pleiotropic phenotypes can arise from simple genetic variation, probably regulatory in nature.
- Published
- 2018
25. Cambrian origin of the CYP27C1-mediated vitamin A1-to-A2 switch, a key mechanism of vertebrate sensory plasticity
- Author
-
M. Carter Cornwall, Ala Morshedian, Stephen D. McCormick, Rikard Frederiksen, Jennifer M. Enright, Gordon L. Fain, Gabriel E. Pollock, Joseph C. Corbo, and Matthew B. Toomey
- Subjects
0301 basic medicine ,Vitamin ,genetic structures ,Period (gene) ,Sensory system ,03 medical and health sciences ,chemistry.chemical_compound ,0302 clinical medicine ,biology.animal ,medicine ,14. Life underwater ,lcsh:Science ,Multidisciplinary ,Retinal pigment epithelium ,biology ,Lamprey ,visual ecology ,Vertebrate ,Biology (Whole Organism) ,Anatomy ,biology.organism_classification ,photoreceptor ,030104 developmental biology ,medicine.anatomical_structure ,Petromyzon ,chemistry ,Rhodopsin ,Evolutionary biology ,Petromyzon marinus ,biology.protein ,lcsh:Q ,sense organs ,030217 neurology & neurosurgery ,Research Article - Abstract
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 A 1 into vitamin A 2 , thereby shifting the ratio of vitamin A 1 -based rhodopsin to red-shifted vitamin A 2 -based porphyropsin in the eye. Here, we show that the sea lamprey ( Petromyzon marinus ), a jawless vertebrate that diverged from jawed vertebrates during the Cambrian period (approx. 500 Ma), dynamically shifts its photoreceptor spectral sensitivity via vitamin A 1 -to-A 2 chromophore exchange as it transitions between photically divergent aquatic habitats. We further show that this shift correlates with high-level expression of the lamprey orthologue of CYP27C1, specifically in the retinal pigment epithelium as in jawed vertebrates. Our results suggest that the CYP27C1-mediated vitamin A 1 -to-A 2 switch is an evolutionarily ancient mechanism of sensory plasticity that appeared not long after the origin of vertebrates.
- Published
- 2017
26. A non-coding region near Follistatin controls head colour polymorphism in the Gouldian finch
- Author
-
Pedro Araújo, Cristiana I. Marques, Matthew B. Toomey, Joseph C. Corbo, Miguel Carneiro, Stephen J. Sabatino, Małgorzata Anna Gazda, Ricardo Lopes, Pedro Andrade, and Sandra Afonso
- Subjects
0301 basic medicine ,education.field_of_study ,General Immunology and Microbiology ,biology ,Range (biology) ,Population ,General Medicine ,Balancing selection ,General Biochemistry, Genetics and Molecular Biology ,03 medical and health sciences ,030104 developmental biology ,Pleiotropy ,Polymorphism (computer science) ,Sympatric speciation ,Evolutionary biology ,biology.protein ,Coding region ,General Agricultural and Biological Sciences ,education ,General Environmental Science ,Follistatin - Abstract
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 differences and the factors that promote the long-term maintenance of phenotypic variability within a freely interbreeding population are incomplete. Here, we investigated the genetic basis of red and black head colour in the Gouldian finch ( Erythrura gouldiae ), a classic polymorphic system in which naturally occurring colour morphs also display differences in aggressivity and reproductive success. We show that the candidate locus is a small (approx. 70 kb) non-coding region mapping to the Z chromosome near the Follistatin ( FST ) gene. Unlike recent findings in other systems where phenotypic morphs are explained by large inversions containing hundreds of genes (so-called supergenes), we did not identify any structural rearrangements between the two haplotypes using linked-read sequencing technology. Nucleotide divergence between the red and black alleles was high when compared to the remainder of the Z chromosome, consistent with their maintenance as balanced polymorphisms over several million years. Our results illustrate how pleiotropic phenotypes can arise from simple genetic variation, probably regulatory in nature.
- Published
- 2018
27. Genetic basis for red coloration in birds
- Author
-
Ricardo Lopes, James D. Johnson, Geoffrey E. Hill, Matthew B. Toomey, Pedro Araújo, Leif Andersson, Miguel Carneiro, José Melo-Ferreira, Joseph C. Corbo, and Mafalda S. Ferreira
- Subjects
0106 biological sciences ,0301 basic medicine ,food.ingredient ,Canaries ,Zoology ,010603 evolutionary biology ,01 natural sciences ,General Biochemistry, Genetics and Molecular Biology ,Retina ,Article ,Transcriptome ,Avian Proteins ,03 medical and health sciences ,Pigment ,food ,Cytochrome P-450 Enzyme System ,biology.animal ,Skin Physiological Phenomena ,Botany ,Animals ,Carotenoid ,Gene ,chemistry.chemical_classification ,biology ,Pigmentation ,Spinus ,Pigments, Biological ,Feathers ,030104 developmental biology ,chemistry ,Mate choice ,Liver ,visual_art ,Feather ,visual_art.visual_art_medium ,Finches ,General Agricultural and Biological Sciences ,Serinus canaria - Abstract
Summary 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 for red coloration in birds using whole-genome sequencing of red siskins ( Spinus cucullata ), common canaries ( Serinus canaria ), and "red factor" canaries, which are the hybrid product of crossing red siskins with common canaries [7]. We identified two genomic regions introgressed from red siskins into red factor canaries that are required for red coloration. One of these regions contains a gene encoding a cytochrome P450 enzyme, CYP2J19 . Transcriptome analysis demonstrates that CYP2J19 is significantly upregulated in the skin and liver of red factor canaries, strongly implicating CYP2J19 as the ketolase that mediates red coloration in birds. Interestingly, a second introgressed region required for red feathers resides within the epidermal differentiation complex, a cluster of genes involved in development of the integument. Lastly, we present evidence that CYP2J19 is involved in ketocarotenoid formation in the retina. The discovery of the carotenoid ketolase has important implications for understanding sensory function and signaling mediated by carotenoid pigmentation.
- Published
- 2016
28. Author response: Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds
- Author
-
Nicholas W. Roberts, Steven J. Schwartz, Misha Vorobyev, Christopher C. Witt, David Wilby, Ken M. Riedl, Robert W. Curley, Matthew B. Toomey, Olle Lind, Joseph C. Corbo, Earl H. Harrison, Kevin J. McGraw, Rikard Frederiksen, M. Carter Cornwall, and Almut Kelber
- Subjects
Physics ,Optics ,business.industry ,medicine ,Adaptive potential ,medicine.disease_cause ,business ,Ultraviolet - Published
- 2016
29. The effects of sun exposure on carotenoid accumulation and oxidative stress in the retina of the House Finch (Haemorhous mexicanus)
- Author
-
Kevin J. McGraw and Matthew B. Toomey
- Subjects
0106 biological sciences ,0301 basic medicine ,Zoology ,macromolecular substances ,Biology ,medicine.disease_cause ,010603 evolutionary biology ,01 natural sciences ,Intraspecific competition ,Lipid peroxidation ,03 medical and health sciences ,chemistry.chemical_compound ,biology.animal ,Botany ,polycyclic compounds ,medicine ,Carotenoid ,Ecology, Evolution, Behavior and Systematics ,chemistry.chemical_classification ,Sunlight ,organic chemicals ,food and beverages ,Retinal ,biological factors ,Quail ,030104 developmental biology ,chemistry ,Photoprotection ,Animal Science and Zoology ,Oxidative stress - Abstract
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 not known if or how wild birds respond to ecologically relevant variation in sun exposure. We manipulated the duration of natural sunlight exposure and dietary carotenoid levels in wild-caught captive House Finches (Haemorhous mexicanus), then measured carotenoid accumulation and oxidative stress in the retina. We found no significant effects of sun exposure on retinal levels of carotenoids or lipid peroxidation, in replicate experiments, in winter (Jan–Mar) and spring/summer (May–June). Dietary carotenoid supplementation in the spring/summer experiment led to significantly higher retinal carotenoid levels, but did not affect lipid peroxidation. Carotenoid levels differed significantly between the winter and spring/summer experiments, with higher retinal and lower plasma carotenoid levels in birds from the later experiment. Our results suggest that variation in the duration of exposure to direct sunlight have limited influence on intraspecific variation in retinal carotenoid accumulation, but that accumulation may track other seasonal–environmental cues and physiological processes.
- Published
- 2016
30. Food color preferences against a dark, textured background vary in relation to sex and age in house finches (Carpodacus mexicanus)
- Author
-
Michael W. Butler, Matthew B. Toomey, Hirbod Behbahaninia, and Kevin J. McGraw
- Subjects
genetic structures ,Adult male ,Ecology ,Foraging ,Zoology ,Orange (colour) ,Biology ,Behavioral Neuroscience ,Chromatic contrast ,Food color ,Green food ,Plumage ,Animal Science and Zoology ,Carpodacus mexicanus - Abstract
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 example, showed that individuals preferred red and green food items and avoided yellow ones. However, this study of desert, ground-feeding birds was done with seeds presented against an artificial white background that is unlikely to reflect natural conditions. Therefore, we performed a similar experiment, but quantified selection of colorful foods using a different visual environment that better mimicked natural conditions. We mixed dark, inedible distractor pellets (i.e., analogous to natural desert sand and rocks) with sunflower kernels that were colored red, green, yellow, or orange to test for differences in foraging patterns by sex, age, and expression of male plumage coloration in non-molting house finches. This food presentation resulted in yellow seeds having a significantly greater chromatic, but not achromatic, contrast with the background than red or green seeds. Under these conditions, all birds consumed yellow, and to a lesser extent red, seeds most often, and both adult males and females had a strong preference for yellow kernels; adult males also tended to prefer green kernels, but females tended not to prefer green kernels. Juveniles showed no significant preferences for any seed color, and adult male plumage coloration was not related to seed color preference. Therefore, in contrast to studies using different foraging environments, house finches tended to prefer yellow seeds, supporting models that suggest that visual background and contrast may be more important than color per se in visually mediated foraging decisions of birds. Moreover, the fact that adult males and females differed in food color preference has not been reported previously in songbirds.
- Published
- 2012
31. Naturally high plasma glucose levels in mourning doves (Zenaida macroura) do not lead to high levels of reactive oxygen species in the vasculature
- Author
-
Eldon J. Braun, Karen L. Sweazea, Christina L. Smith, Blair O. Wolf, Benjimen R. Walker, Matthew B. Toomey, and Kevin J. McGraw
- Subjects
Blood Glucose ,Male ,medicine.medical_specialty ,Antioxidant ,medicine.medical_treatment ,Xanthophylls ,Biology ,medicine.disease_cause ,Article ,Antioxidants ,Fluorescence ,Superoxide dismutase ,chemistry.chemical_compound ,Zeaxanthins ,Internal medicine ,medicine ,Animals ,Vitamin E ,Columbidae ,Mesenteric arteries ,chemistry.chemical_classification ,Reactive oxygen species ,Superoxide Dismutase ,Lutein ,Catalase ,Mesenteric Arteries ,Uric Acid ,Endocrinology ,medicine.anatomical_structure ,chemistry ,biology.protein ,Uric acid ,Animal Science and Zoology ,Reactive Oxygen Species ,Oxidative stress - Abstract
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) levels in birds, they appear resistant to the development of oxidative stress in tissues such as the heart, brain and kidneys. To our knowledge no information exists on oxidative stress susceptibility in the resistance vasculature of birds. Therefore, we compared endogenous antioxidant mechanisms in the resistance vasculature of mourning doves (MODO; Zenaida macroura) and rats (Rattus norvegicus). Reactive oxygen species (ROS) were assessed with the fluorescent indicator 7'-dichlorodihydrofluorescein diacetate, acetyl ester in mesenteric arteries from rats and wild-caught MODO. Despite having significantly higher P(Glu) than rats, there were no significant differences in ROS levels between mesenteric arteries from rats or doves. Although superoxide dismutase and catalase activities were lower in the plasma, total antioxidant capacity, uric acid, vitamin E (α-tocopherol), and carotenoids (lutein and zeaxanthin) were significantly higher in MODO than in rats. Thus, compared to rats, MODO have multiple circulating antioxidants that may prevent the development of oxidative stress in the vasculature.
- Published
- 2011
32. How many color metrics do we need? Evaluating how different color-scoring procedures explain carotenoid pigment content in avian bare-part and plumage ornaments
- Author
-
Michael W. Butler, Kevin J. McGraw, and Matthew B. Toomey
- Subjects
Brightness ,Ecology ,Zoology ,Biology ,Color space ,Pigment ,Beak ,Animal ecology ,Plumage ,visual_art ,visual_art.visual_art_medium ,Animal Science and Zoology ,Zebra finch ,Ecology, Evolution, Behavior and Systematics ,Hue - Abstract
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 tested systematically. Here, we examined which commonly employed color metrics predict carotenoid content of ornaments in three avian species (house finch Carpodacus mexicanus, mallard duck Anas platyrhynchos, and zebra finch Taeniopygia guttata). We used spectrophotometry to measure reflectance spectra from beak and feather tissue, calculated numerous color metrics (e.g., hue, chroma, brightness, principal components, and tetrahedral color space position) from these spectra, and determined carotenoid content at the site of color measurement with high-performance liquid chromatography. We found that several principal component, tristimulus, and avian visual model metrics significantly correlated with carotenoid content of house finch feathers and duck beaks. Carotenoid content of mallard beaks was most closely correlated with brightness and saturation metrics, whereas in house finch feathers, carotenoid concentration was best captured by hue and saturation metrics. According to tristimulus scores and visual models, we found that the ultraviolet portion of the spectrum was not an essential predictor of variation in carotenoid content. Also, visual model chromatic contrasts generally were not significant predictors of carotenoid content, although some achromatic contrasts and tetrahedral color space vector parameters were. Our results indicate that numerous methods, especially tristimulus scores, are suitable for capturing pigment-based color variation in two carotenoid-containing ornaments, and we discuss the merits and shortcomings of these different approaches. In contrast, there were no significant relationships between any color metrics and the carotenoid content of zebra finch beaks, suggesting that other color-generating mechanisms besides carotenoids may contribute to color variability in this species.
- Published
- 2010
33. A novel method for quantifying the glossiness of animals
- Author
-
Matthew B. Toomey, Lisa A. Taylor, Kevin J. McGraw, Michael W. Butler, Melissa G. Meadows, and H. Bobby Fokidis
- Subjects
biology ,Ecology ,Zoology ,Context (language use) ,biology.organism_classification ,Iridescence ,Quiscalus ,Sexual dimorphism ,Animal ecology ,Plumage ,Sexual selection ,Grackle ,Animal Science and Zoology ,Ecology, Evolution, Behavior and Systematics - Abstract
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 undertook two studies of glossiness in avian plumage to determine (a) the repeatability of a recently developed measure of glossiness, (b) the relationship between glossiness and conventional measures of coloration, and (c) how glossiness is associated with quality signaling. Using museum specimens of three North American bird species with glossy plumage (red-winged blackbird, Agelaius phoeniceus; great-tailed grackle, Quiscalus mexicanus; Chihuahuan raven, Corvus cryptoleucus), we found that the glossiness measure was highly repeatable for all species and was significantly correlated with plumage coloration (e.g., chroma, brightness) in male great-tailed grackles. We then used wild-caught grackles to examine sexual dimorphism in plumage glossiness and its correlation to a potentially sexually selected trait in this species, male tail length. We found that males were significantly glossier than females and that male, but not female, glossiness correlated positively with tail length. This study provides a repeatable method to measure glossiness and highlights its potential as a signal of individual quality in animals.
- Published
- 2010
34. Carotenoid Accumulation in the Tissues of Zebra Finches: Predictors of Integumentary Pigmentation and Implications for Carotenoid Allocation Strategies
- Author
-
Kevin J. McGraw and Matthew B. Toomey
- Subjects
Male ,food.ingredient ,Physiology ,Color ,Adipose tissue ,Zoology ,Context (language use) ,Biology ,Biochemistry ,Retina ,food ,Yolk ,Botany ,Animals ,Carotenoid ,Chromatography, High Pressure Liquid ,chemistry.chemical_classification ,Pigmentation ,Sexual attraction ,Beak ,food and beverages ,Integumentary system ,Carotenoids ,Liver metabolism ,Adipose Tissue ,Liver ,chemistry ,Photoprotection ,Female ,Animal Science and Zoology ,Finches - Abstract
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 in numerous internal body tissues (e.g., liver, adipose tissue, retina) whose carotenoid types and amounts are rarely studied in the context of color acquisition. Because male and female animals typically place different priorities on fitness-enhancing activities (e.g., gametic investment in females, sexual attraction in males), carotenoid allocation may track such investment patterns in the two sexes, and we can test for such sex-specific priorities of carotenoids by assessing body-tissue distributions of these pigments. We used high-performance liquid chromatography to identify and quantify carotenoid pigments from the plasma, liver, adipose tissue, and retina as well as the beak and legs of male and female zebra finches (Taeniopygia guttata), a species in which males display sexually attractive, red, carotenoid-based beak coloration and females also display some (albeit a less rich orange) beak color. To our knowledge, this is the first study of the predictors of carotenoid-based leg coloration-another potentially important visual signal-in this species. The same suite of dietary (e.g., lutein, zeaxanthin, beta-cryptoxanthin) and metabolically derived (e.g., dehydrolutein, anhydrolutein) yellow and orange carotenoids was present in plasma, liver, and adipose tissue of both sexes. Retina contained two different metabolites (astaxanthin and galloxanthin) that serve specific functions in association with unique photoreceptor types in the eye. Beaks were enriched with four red ketocarotenoid derivatives in both sexes (alpha-doradexanthin, adonirubin, astaxanthin, and canthaxanthin), while the carotenoid profile of legs was similar to that of plasma/liver/adipose tissue but with the additional presence of canthaxanthin. Sex differences in beak coloration were attributable to different concentrations of all four red ketocarotenoids. Males also had more colorful legs than did females, and this color difference was due to the increased presence of canthaxanthin in males. Males had higher carotenoid concentrations in plasma and retina than did females, but females had higher carotenoid concentrations in liver and adipose tissue than did males. These patterns are consistent with the apparently different life-history strategies employed for carotenoids by adult males and females, with females prioritizing future access to carotenoids (in tissue stores for egg production) and males prioritizing current access (in circulation, for maintaining bright color and/or health).
- Published
- 2010
35. Food Color Preferences of Molting House Finches (Carpodacus mexicanus) in Relation to Sex and Plumage Coloration
- Author
-
Elizabeth A. Tourville, Ana L. Bascuñán, Matthew B. Toomey, and Kevin J. McGraw
- Subjects
genetic structures ,Plumage ,Ecology ,Foraging ,Color preferences ,Food choice ,Captivity ,Juvenile ,Animal Science and Zoology ,Orange (colour) ,Biology ,Moulting ,Ecology, Evolution, Behavior and Systematics - Abstract
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 with (or growing) more colorful ornaments show stronger food-color preferences than those with drabber coloration. Here, we examine food color preferences in house finches (Carpodacus mexicanus) ‐ a species with sexually dichromatic and selected carotenoid coloration ‐ as a function of sex and plumage coloration during molt. We captured wild, molting juvenile house finches over 4 wk in late summer ⁄early fall, quantified the color and size of plumage ornaments being developed in males, and determined food color preference in captivity by presenting individuals with dyed sunflower chips (red, orange, yellow, and green). On average, finches showed an aversion to yellow-dyed chips and a preference for red- and green-colored chips. We found no significant difference between male and female preferences for specific food colors, and food color preference was not significantly related to male plumage ornamentation. However, we did find that redder birds demonstrated a higher degree of food selectivity, measured as the proportion of their preferred food color consumed. These results suggest that food color is not a major factor determining food choice in molting house finches, but that there still may be aspects of foraging behavior that are linked to the development of colorful plumage.
- Published
- 2009
36. Seasonal, sexual, and quality related variation in retinal carotenoid accumulation in the house finch (Carpodacus mexicanus)
- Author
-
Kevin J. McGraw and Matthew B. Toomey
- Subjects
chemistry.chemical_classification ,education.field_of_study ,Retina ,genetic structures ,biology ,organic chemicals ,Population ,food and beverages ,Zoology ,Retinal ,macromolecular substances ,Zeaxanthin ,chemistry.chemical_compound ,medicine.anatomical_structure ,chemistry ,Plumage ,Photoprotection ,biology.animal ,Botany ,medicine ,education ,Carotenoid ,Ecology, Evolution, Behavior and Systematics ,Finch - Abstract
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 photoprotection and tune colour vision. In domesticated species, carotenoid accumulation in retina is dependent on dietary intake, but little is known about the variability in or control of these pigments in the eyes of wild animals. 3. Carotenoids are also deposited in the integument of many animals, where they generate colourful sexually selected displays that communicate information about individual health and nutrition. We hypothesize that retinal carotenoid accumulation is subject to the same health and nutritional constraints as the use of carotenoids in colour signals. 4. As a first test of this hypothesis, we examined retinal carotenoid accumulation in relation to season, sex, body condition, circulating plasma carotenoid concentrations, and plumage colouration in a free ranging population of house finches ( Carpodacus mexicanus ) ‐ a model species for studies of carotenoid ecology. 5. Retinal carotenoid accumulation varied considerably among individuals and differed significantly among seasons, with the highest levels observed in late fall and winter. Body condition and plasma zeaxanthin levels were significantly positively correlated with retinal carotenoid accumulation, but retinal carotenoid concentrations did not differ between the sexes. Plumage redness covaried positively with retinal carotenoid concentration as well, though this relationship was no longer significant when accounting for seasonal variation. 6. Our results, although correlational, do suggest that retinal carotenoid accumulation is a variable trait that may be influenced by environmental and physiological conditions, raising the intriguing possibility that plumage colouration and colour vision could be linked through a common biochemical mechanism.
- Published
- 2009
37. The Effects of Social Context on the Food-Caching Behavior of Florida Scrub-Jays (Aphelocoma coerulescens)
- Author
-
Reed Bowman, Glen E. Woolfenden, and Matthew B. Toomey
- Subjects
Adaptive value ,biology ,Florida scrub ,Ecology ,Cooperative breeding ,Breeding pair ,Social environment ,Animal Science and Zoology ,Provisioning ,Cache ,biology.organism_classification ,Ecology, Evolution, Behavior and Systematics ,Aphelocoma - Abstract
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 harvesting experimentally provisioned peanuts alone and in the presence of other family members, to determine whether jays modify their food-handling behavior relative to social context. Non-breeding helpers were less likely to cache in the presence of the dominant male breeder than when alone and all jays tended to cache out of sight when observed by another jay. These changes in caching behavior are consistent with cache protection strategies employed by other species. However, the adaptive value of such cache protection within a sedentary cooperatively breeding family group on a year-round territory is unclear.
- Published
- 2007
38. Factors affecting the movement of adult zebra mussels (Dreissena polymorpha)
- Author
-
Matthew B. Toomey, J. E. Marsden, and Declan J. McCabe
- Subjects
Fishery ,biology ,Byssus ,Thin layer ,Zebra mussel ,Aquatic Science ,biology.organism_classification ,Dreissena ,Ecology, Evolution, Behavior and Systematics - Abstract
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. Mussels were placed in aquaria and their movement was recorded after a 2-h interval. Mussels left visible trails in a thin layer of sand on the aquarium floor that allowed for accurate measurements of distance and direction of movement. The tendency to move and distance moved by the mussels was inversely proportional to size of the individual mussels. There was no significant effect of temperature on movement, though smaller mussels tended to move more at higher temperatures. Although distance traveled was not significantly different in light versus dark conditions, there was a significant effect of light on direction traveled. Zebra mussels were strongly ne...
- Published
- 2002
39. Testosterone influences the accumulation of carotenoids in the retina of a wild bird (39.4)
- Author
-
Matthew B. Toomey, Kevin J. McGraw, Scott Davies, and Chelsie Daniel
- Subjects
chemistry.chemical_classification ,medicine.medical_specialty ,Retina ,animal structures ,Zoology ,Biology ,Biochemistry ,Spectral sensitivity ,Endocrinology ,medicine.anatomical_structure ,chemistry ,Internal medicine ,Genetics ,medicine ,Molecular Biology ,Carotenoid ,Testosterone ,Biotechnology - Abstract
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 finch...
- Published
- 2014
40. Ketocarotenoid circulation, but not retinal carotenoid accumulation, is linked to eye disease status in a wild songbird
- Author
-
Kevin J. McGraw, Molly Staley, Geoffrey E. Hill, Matthew B. Toomey, Mathieu Giraudeau, School of Life Sciences [Tempe, USA], Arizona State University [Tempe] (ASU), Auburn University (AU), Washington University School of Medicine in St. Louis, and Washington University in Saint Louis (WUSTL)
- Subjects
0106 biological sciences ,Mycoplasma gallisepticum ,Male ,[SDV]Life Sciences [q-bio] ,Biophysics ,Zoology ,Down-Regulation ,Haemorhous mexicanus ,Disease ,010603 evolutionary biology ,01 natural sciences ,Biochemistry ,Plumage ,03 medical and health sciences ,chemistry.chemical_compound ,Immune system ,Retinal Diseases ,Retina ,Botany ,medicine ,Animals ,Scattering, Radiation ,Molecular Biology ,Carotenoid ,030304 developmental biology ,chemistry.chemical_classification ,0303 health sciences ,Photolysis ,biology ,food and beverages ,Retinal ,House finch ,medicine.disease ,biology.organism_classification ,Conjunctivitis ,Carotenoids ,Songbird ,Coccidiosis ,Disease Models, Animal ,chemistry ,Oxidative stress ,Finches ,Photic Stimulation - Abstract
International audience; Pathogenic or parasitic infections pose numerous physiological challenges to organisms. Carotenoid pigments have often been used as biomarkers of disease state and impact because they integrate multiple aspects of an individual's condition and nutritional and health state. Some diseases are known to influence carotenoid uptake from food (e.g. coccidiosis) and carotenoid use (e.g. as antioxidants/immunostimulants in the body, or for sexually attractive coloration), but there is relatively little information in animals about how different types of carotenoids from different tissue sources may be affected by disease. Here we tracked carotenoid accumulation in two body pools (retina and plasma) as a function of disease state in free-ranging house finches (Haemorhous mexicanus). House finches in eastern North America can contract mycoplasmal conjunctivitis (Mycoplasma gallisepticum, or MG), which can progress from eye swelling to eye closure and death. Previous work showed that systemic immune challenges in house finches lower carotenoid levels in retina, where they act as photoprotectors and visual filters. We assessed carotenoid levels during the molt period, a time of year when finches uniquely metabolize ketocarotenoids (e.g. 3-hydroxy-echinenone) for acquisition of sexually selected red plumage coloration, and found that males infected with MG circulated significantly lower levels of 3-hydroxy-echinenone, but no other plasma carotenoid types, than birds exhibiting no MG symptoms. This result uncovers a key biochemical mechanism for the documented detrimental effect of MG on plumage redness in H. mexicanus. In contrast, we failed to find a relationship between MG infection status and retinal carotenoid concentrations. Thus, we reveal differential effects of an infectious eye disease on carotenoid types and tissue pools in a wild songbird. At least compared to retinal sources (which appear somewhat more temporally stable than other body carotenoid pools, even to diseases of the eye evidently), our results point to either a high physiological cost of ketocarotenoid synthesis (as is argued in models of sexually selected carotenoid coloration) or high benefit of using this ketocarotenoid to combat infection.
- Published
- 2013
41. Can House Finches (Carpodacus mexicanus) use non-visual cues to discriminate the carotenoid content of foods?
- Author
-
Kevin J. McGraw, Matthew B. Toomey, Mathieu Giraudeau, School of Life Sciences [Tempe, USA], Arizona State University [Tempe] (ASU), Washington University School of Medicine in St. Louis, and Washington University in Saint Louis (WUSTL)
- Subjects
0106 biological sciences ,chemistry.chemical_classification ,Taste ,[SDV]Life Sciences [q-bio] ,05 social sciences ,Foraging ,Zoology ,food and beverages ,Olfaction ,Biology ,010603 evolutionary biology ,01 natural sciences ,Carotenoids ,House Finch ,Odor ,chemistry ,Plumage ,Botany ,0501 psychology and cognitive sciences ,050102 behavioral science & comparative psychology ,Sensory cue ,Carotenoid ,Flavor - Abstract
International audience; 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 this hypothesis, it was recently found that birds can discriminate between carotenoid-enriched diets and control diets, even if both have the same color, suggesting that there may be underlying non-visual (e.g., olfactory, taste) mechanisms for detecting carotenoid presence or enrichment in foods. In this study, we performed two experiments with male House Finches (Carpodacus mexicanus) to test if this species is able to discriminate between (1) carotenoid-enriched and plain sunflower seeds (while controlling for food coloration), and (2) plain seeds scented with β-ionone, which is a carotenoid-degradation product that is common in many fruits and is one of the most powerful flavor-active organic compounds, or a sham odorant. We found that finches did not show significant food preferences in either experiment, indicating that they did not use odor or flavor cues associated with carotenoids to discriminate between foods. However, our results do not rule out the possibilities that other flavors or odors can be used in discrimination or that finches may learn to discriminate flavors and odors over longer periods of time or at other times of year through post-ingestive feedback mechanisms.
- Published
- 2012
42. A complex carotenoid palette tunes avian colour vision
- Author
-
M. Carter Cornwall, Matthew B. Toomey, Rikard Frederiksen, Joseph C. Corbo, Aaron M. Collins, and Jerilyn A. Timlin
- Subjects
Light ,genetic structures ,Ultraviolet Rays ,Color vision ,Biomedical Engineering ,Biophysics ,Color ,Bioengineering ,Xanthophylls ,Biology ,Biochemistry ,Retinal Cone Photoreceptor Cells ,Retina ,Biomaterials ,chemistry.chemical_compound ,Zeaxanthins ,Astaxanthin ,Animals ,Carotenoid ,Research Articles ,Chromatography, High Pressure Liquid ,chemistry.chemical_classification ,Chromatography ,Color Vision ,Pigmentation ,Lutein ,food and beverages ,Carotenoids ,eye diseases ,Zeaxanthin ,Spectral sensitivity ,chemistry ,Microspectrophotometry ,Xanthophyll ,Oil droplet ,sense organs ,Biological system ,Chickens ,Oils ,Biotechnology - Abstract
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 composition has remained uncertain owing to the technical challenges of measuring these very small, dense and highly refractile optical organelles. In this study, we integrated results from high-performance liquid chromatography, hyperspectral microscopy and microspectrophotometry to obtain a comprehensive understanding of oil droplet carotenoid pigmentation in the chicken (Gallus gallus). We find that each of the four carotenoid-containing droplet types consists of a complex mixture of carotenoids, with a single predominant carotenoid determining the wavelength of the spectral filtering cut-off. Consistent with previous reports, we find that the predominant carotenoid type in the oil droplets of long-wavelength-sensitive, medium-wavelength-sensitive and short-wavelength-sensitive type 2 cones are astaxanthin, zeaxanthin and galloxanthin, respectively. In addition, the oil droplet of the principal member of the double cone contains a mixture of galloxanthin and two hydroxycarotenoids (lutein and zeaxanthin). Short-wavelength-absorbing apocarotenoids are present in all of the droplet types, providing filtering of light in a region of the spectrum where filtering by hydroxy- and ketocarotenoids may be incomplete. Thus, birds rely on a complex palette of carotenoid pigments within their cone oil droplets to achieve finely tuned spectral filtering.
- Published
- 2015
43. Ontogenetic immune challenges shape adult personality in mallard ducks
- Author
-
Kevin J. McGraw, Michael W. Butler, Matthew B. Toomey, and Melissah Rowe
- Subjects
Anas ,Male ,media_common.quotation_subject ,Ontogeny ,Personality development ,General Biochemistry, Genetics and Molecular Biology ,Developmental psychology ,Personality ,Animals ,Big Five personality traits ,Research Articles ,General Environmental Science ,media_common ,General Immunology and Microbiology ,biology ,Behavior, Animal ,Age Factors ,Erikson's stages of psychosocial development ,General Medicine ,biology.organism_classification ,Immunity, Innate ,Immunity, Humoral ,Ducks ,Plumage ,Developmental plasticity ,General Agricultural and Biological Sciences - Abstract
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 of adult personality. We examined how non-pathogenic immune challenges, administered at different stages of development, affected two common measures of personality, activity and exploratory behaviour, as well as colour-dependent novel object exploration in adult male mallard ducks ( Anas platyrhynchos ). We found that individuals that were immune-challenged during the middle (immediately following the completion of somatic growth) and late (during the acquisition of nuptial plumage) stages of development were more active in novel environments as adults relative to developmentally unchallenged birds or those challenged at an earlier developmental time point. Additionally, individuals challenged during the middle stage of development preferred orange and avoided red objects more than those that were not immune-challenged during development. Our results demonstrate that, in accordance with our predictions, early-life immune system perturbations alter the expression of personality traits later in life, emphasizing the role that developmental plasticity plays in shaping adult personality, and lending support to recent theoretical models that suggest that parasite pressure may play an important role in animal personality development.
- Published
- 2011
44. The effects of dietary carotenoid supplementation and retinal carotenoid accumulation on vision-mediated foraging in the house finch
- Author
-
Kevin J. McGraw and Matthew B. Toomey
- Subjects
0106 biological sciences ,Male ,Animal Nutrition ,Visual System ,lcsh:Medicine ,01 natural sciences ,Color discrimination ,chemistry.chemical_compound ,Behavioral Ecology ,Ornithology ,Passeriformes ,lcsh:Science ,Carotenoid ,Animal Management ,2. Zero hunger ,chemistry.chemical_classification ,0303 health sciences ,Multidisciplinary ,biology ,Behavior, Animal ,Ecology ,Animal Behavior ,food and beverages ,Sensory Systems ,medicine.anatomical_structure ,Medicine ,Female ,Sensory Perception ,Research Article ,Color vision ,Foraging ,Zoology ,Color ,010603 evolutionary biology ,Retina ,03 medical and health sciences ,Food Preferences ,biology.animal ,Botany ,medicine ,Animals ,Biology ,Finch ,Lighting ,Vision, Ocular ,030304 developmental biology ,Nutrition ,Evolutionary Biology ,lcsh:R ,Spectral filtering ,Retinal ,Carotenoids ,chemistry ,Dietary Supplements ,lcsh:Q ,Veterinary Science ,Neuroscience - Abstract
Background 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 varies significantly among individuals and is related to dietary carotenoid intake. If diet-induced changes in retinal carotenoid accumulation alter spectral sensitivity, then they have the potential to affect visually mediated foraging performance. Methodology/Principal Findings In two experiments, we measured foraging performance of house finches with dietarily manipulated retinal carotenoid levels. We tested each bird's ability to extract visually contrasting food items from a matrix of inedible distracters under high-contrast (full) and dimmer low-contrast (red-filtered) lighting conditions. In experiment one, zeaxanthin-supplemented birds had significantly increased retinal carotenoid levels, but declined in foraging performance in the high-contrast condition relative to astaxanthin-supplemented birds that showed no change in retinal carotenoid accumulation. In experiments one and two combined, we found that retinal carotenoid concentrations predicted relative foraging performance in the low- vs. high-contrast light conditions in a curvilinear pattern. Performance was positively correlated with retinal carotenoid accumulation among birds with low to medium levels of accumulation (∼0.5–1.5 µg/retina), but declined among birds with very high levels (>2.0 µg/retina). Conclusion/Significance Our results suggest that carotenoid-mediated spectral filtering enhances color discrimination, but that this improvement is traded off against a reduction in sensitivity that can compromise visual discrimination. Thus, retinal carotenoid levels may be optimized to meet the visual demands of specific behavioral tasks and light environments.
- Published
- 2010
45. Immune-system activation depletes retinal carotenoids in house finches (Carpodacus mexicanus)
- Author
-
Michael W. Butler, Kevin J. McGraw, and Matthew B. Toomey
- Subjects
Male ,Physiology ,Aquatic Science ,Molting ,Retina ,chemistry.chemical_compound ,Immune system ,Immunity ,Animals ,Molecular Biology ,Carotenoid ,Ecology, Evolution, Behavior and Systematics ,Phytohaemagglutinin ,chemistry.chemical_classification ,Analysis of Variance ,biology ,Body Weight ,food and beverages ,Retinal ,Carotenoids ,Zeaxanthin ,chemistry ,Insect Science ,Immune System ,Immunology ,biology.protein ,Animal Science and Zoology ,Female ,Finches ,Antibody ,Moulting - Abstract
SUMMARY 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 unique opportunity to track the costs of immune activation, because they are diet-derived, modulate the immune system, and are used to develop colorful signals of quality. Carotenoids also accumulate in the retinas of birds, where they tune spectral sensitivity and provide photoprotection. If carotenoid accumulation in the retina follows the patterns of other tissues, then immune activation may deplete retinal carotenoid levels and impact visual health and function. To test this hypothesis, we challenged molting wild-caught captive house finches (Carpodacus mexicanus) with weekly injections of lipopolysaccharide (LPS) and phytohaemagglutinin (PHA) over the course of 8 weeks. Immunostimulated adult males and females produced significant antibody responses and molted more slowly than uninjected control birds. After 8 weeks, immune-challenged birds had significantly lower levels of specific retinal carotenoid types (galloxanthin and zeaxanthin), but there were no significant differences in the plasma, liver or feather carotenoid levels between the treatment groups. These results indicate that immune-system activation can specifically deplete retinal carotenoids, which may compromise visual health and performance and represent an additional somatic and behavioral cost of immunity.
- Published
- 2010
46. The effects of dietary carotenoid intake on carotenoid accumulation in the retina of a wild bird, the house finch (Carpodacus mexicanus)
- Author
-
Matthew B. Toomey and Kevin J. McGraw
- Subjects
Male ,Time Factors ,Biophysics ,Zoology ,macromolecular substances ,Biochemistry ,Retina ,chemistry.chemical_compound ,Pigment ,Astaxanthin ,Botany ,polycyclic compounds ,medicine ,Animals ,Passeriformes ,Carpodacus mexicanus ,Molecular Biology ,Carotenoid ,chemistry.chemical_classification ,biology ,Dose-Response Relationship, Drug ,organic chemicals ,food and beverages ,Retinal ,biology.organism_classification ,Carotenoids ,biological factors ,Songbird ,Diet ,Zeaxanthin ,medicine.anatomical_structure ,chemistry ,visual_art ,Dietary Supplements ,visual_art.visual_art_medium ,Housing ,Female - Abstract
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 domesticated species, and the effects of dietary carotenoid access on retinal carotenoid accumulation have not been investigated in any wild animal species. The purpose of our studies was to examine how variation in dietary carotenoid types and levels affect retinal accumulation in house finches ( Carpodacus mexicanus ), a common and colorful North American songbird. We carried out three 8-week studies with wild-caught captive birds: (1) we tracked the rate of retinal carotenoid depletion, compared to other body tissues, on a very low-carotenoid diet, (2) we supplemented birds with two common dietary carotenoids (lutein + zeaxanthin) and measured the effect on retinal accumulation, and (3) we separately supplemented birds with high levels of zeaxanthin – an important dietary precursor for retinal carotenoids – or astaxanthin – a dominant retinal carotenoid not commonly found in the diet (i.e. a metabolic derivative). We found that carotenoids depleted slowly from the retina compared to other tissues, with a significant (∼50%) decline observed only after 8 weeks on a very low-carotenoid diet. Supplementation with lutein + zeaxanthin or zeaxanthin alone significantly increased only retinal galloxanthin and e-carotene levels, while other carotenoid types in the retina remained unaffected. Concentrations of retinal astaxanthin were unaffected by direct dietary supplementation with astaxanthin. These results suggest highly specific mechanisms of retinal carotenoid metabolism and accumulation, as well as differential rates of turnover among retinal carotenoid types, all of which have important implications for visual health maintenance and interventions.
- Published
- 2010
47. Iridescence: views from many angles
- Author
-
Michael W. Butler, Matthew B. Toomey, Nathan I. Morehouse, Lisa A. Taylor, Melissa G. Meadows, Kevin J. McGraw, and Ronald L. Rutowski
- Subjects
Introduction ,Ecology ,Biomedical Engineering ,Biophysics ,Bioengineering ,Biological evolution ,Biology ,Biochemistry ,Iridescence ,Visual arts ,Biomaterials ,Graduate students ,Interdisciplinary communication ,Structural coloration ,Biotechnology - Abstract
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 properties in comparison with other types of colourants found in nature. Scientists from a variety of disciplines study the optics, development, heritability, chemical make-up, origin, evolution, functions and biomimetic technological applications of naturally occurring iridescent colours. For the first time, graduate students at Arizona State University brought together these scientists, along with educators and artists, at ‘Iridescence: more than meets the eye’, a conference to promote interdisciplinary communication and collaboration in the study of iridescent coloration from all of these perspectives. Here, we summarize the outcomes of this conference, introduce the papers that follow in this special journal issue and briefly review the current status of our understanding of iridescence.
- Published
- 2009
48. Modified saponification and HPLC methods for analyzing carotenoids from the retina of quail: implications for its use as a nonprimate model species
- Author
-
Matthew B. Toomey and Kevin J. McGraw
- Subjects
Male ,Lutein ,Potassium Compounds ,medicine.medical_treatment ,Coturnix ,Xanthophylls ,High-performance liquid chromatography ,Models, Biological ,Retina ,chemistry.chemical_compound ,Astaxanthin ,Zeaxanthins ,medicine ,Hydroxides ,Animals ,Humans ,Sodium Hydroxide ,Carotenoid ,Chromatography, High Pressure Liquid ,chemistry.chemical_classification ,Chromatography ,biology ,Hydrolysis ,Carotene ,food and beverages ,biology.organism_classification ,Carotenoids ,Zeaxanthin ,chemistry ,Biochemistry ,Female ,Saponification - Abstract
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 and quantified with reverse-phase high-performance liquid chromatography (HPLC). To assess the effects of saponification conditions on carotenoid recovery from quail retina, we varied base concentration and the total time of saponification across a wide range and again used HPLC to compare carotenoid concentrations among conditions.Astaxanthin and galloxanthin were the dominant carotenoids recovered in the quail retina, along with smaller amounts of five other carotenoids (lutein, zeaxanthin, 3'-epilutein, epsilon-carotene, and an unidentified carotenoid). Astaxanthin was sensitive to saponification conditions; recovery was poor with strong bases (0.2 and 0.5 M KOH) and best with weak bases (0.01 and 0.2 M KOH). In contrast, xanthophyll carotenoids (galloxanthin, zeaxanthin, lutein, 3'-epilutein, and the unknown) were best recovered with strong base after 6 hours of saponification at room temperature. The recovery of epsilon-carotene was not affected by saponification conditions.Separate chemical hydrolysis procedures--using a strong base to recover xanthophylls and a weak base to recover astaxanthin--should be used for maximizing recovery of quail retinal carotenoids. Because the dominant carotenoids in quail retina are absent in human retina, and because of their different packaging (e.g., esterified in oil droplets) and light-absorbance properties compared with xanthophylls in the human eye, use of the quail as a model organism for studying human retinal carotenoids should be approached with caution.
- Published
- 2007
49. A description of unique fluorescent yellow pigments in penguin feathers
- Author
-
Matthew B. Toomey, Kevin J. McGraw, Melanie Massaro, Nathan I. Morehouse, Pierre Jouventin, and Paul M. Nolan
- Subjects
Ecology ,Spectrophotometry ,Animals ,General Medicine ,Pigments, Biological ,Biology ,Feathers ,Biological sciences ,Archaeology ,Spheniscidae ,Fluorescence ,Pterins - Abstract
School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA Department of Biology, The Citadel, Charleston, SC 29409, USA School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand Centre d’Ecologie Fonctionnelle et Evolutive, Centre National de la Recherche Scientifique, 1919 Route de Mende, Montpellier, France *Address correspondence to Kevin McGraw, e-mail: kevin.mcgraw@asu.edu
- Published
- 2007
50. Mate choice for a male carotenoid-based ornament is linked to female dietary carotenoid intake and accumulation
- Author
-
Kevin J. McGraw and Matthew B. Toomey
- Subjects
Male ,0106 biological sciences ,Evolution ,media_common.quotation_subject ,Zoology ,macromolecular substances ,Biology ,010603 evolutionary biology ,01 natural sciences ,03 medical and health sciences ,QH359-425 ,polycyclic compounds ,Seasonal breeder ,Animals ,Mating ,10. No inequality ,Carotenoid ,Ecology, Evolution, Behavior and Systematics ,030304 developmental biology ,media_common ,chemistry.chemical_classification ,0303 health sciences ,Ecology ,organic chemicals ,Assortative mating ,food and beverages ,Mating Preference, Animal ,Carotenoids ,biological factors ,Preference ,Diet ,chemistry ,Mate choice ,Plumage ,Female ,Finches ,Reproduction ,Research Article - Abstract
Background 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 coloration and a primary mechanism maintaining the honest information content of these signals. Carotenoids also influence female health and reproduction in ways that may alter the costs and benefits of mate choice behaviours and thus provide a potential biochemical link between the expression of male traits and female preferences. To test this hypothesis, we manipulated the dietary carotenoid levels of captive female house finches (Carpodacus mexicanus) and assessed their mate choice behavior in response to color-manipulated male finches. Results Females preferred to associate with red males, but carotenoid supplementation did not influence the direction or strength of this preference. Females receiving a low-carotenoid diet were less responsive to males in general, and discrimination among the colorful males was positively linked to female plasma carotenoid levels at the beginning of the study when the diet of all birds was carotenoid-limited. Conclusions Although female preference for red males was not influenced by carotenoid intake, changes in mating responsiveness and discrimination linked to female carotenoid status may alter how this preference is translated into choice. The reddest males, with the most carotenoid rich plumage, tend to pair early in the breeding season. If carotenoid-related variations in female choice behaviour shift the timing of pairing, then they have the potential to promote assortative mating by carotenoid status and drive the evolution of carotenoid-based male plumage coloration.
- Published
- 2012
Catalog
Discovery Service for Jio Institute Digital Library
For full access to our library's resources, please sign in.