A complex carotenoid palette tunes avian color vision.
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 themore »
- Authors:
-
- Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
- Washington Univ. School of Medicine, St. Louis, MO (United States)
- Sandia National Lab. (SNL-NM), Albuquerque, NM (United States); Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Boston Univ. School of Medicine, Boston, MA (United States)
- Publication Date:
- Research Org.:
- Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1236232
- Report Number(s):
- SAND-2015-4230J
Journal ID: ISSN 1742-5689; 590324
- Grant/Contract Number:
- AC04-94AL85000
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of the Royal Society Interface
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 111; Journal ID: ISSN 1742-5689
- Publisher:
- The Royal Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Timlin, Jerilyn A., Toomey, Matthew B., Collins, Aaron M., Frederiksen, Rikard, Cornwall, M. Carter, and Corbo, Joseph C. A complex carotenoid palette tunes avian color vision.. United States: N. p., 2015.
Web. doi:10.1098/rsif.2015.0563.
Timlin, Jerilyn A., Toomey, Matthew B., Collins, Aaron M., Frederiksen, Rikard, Cornwall, M. Carter, & Corbo, Joseph C. A complex carotenoid palette tunes avian color vision.. United States. doi:https://doi.org/10.1098/rsif.2015.0563
Timlin, Jerilyn A., Toomey, Matthew B., Collins, Aaron M., Frederiksen, Rikard, Cornwall, M. Carter, and Corbo, Joseph C. Wed .
"A complex carotenoid palette tunes avian color vision.". United States. doi:https://doi.org/10.1098/rsif.2015.0563. https://www.osti.gov/servlets/purl/1236232.
@article{osti_1236232,
title = {A complex carotenoid palette tunes avian color vision.},
author = {Timlin, Jerilyn A. and Toomey, Matthew B. and Collins, Aaron M. and Frederiksen, Rikard and Cornwall, M. Carter and Corbo, Joseph C.},
abstractNote = {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. Furthermore, birds rely on a complex palette of carotenoid pigments within their cone oil droplets to achieve finely tuned spectral filtering.},
doi = {10.1098/rsif.2015.0563},
journal = {Journal of the Royal Society Interface},
number = 111,
volume = 12,
place = {United States},
year = {2015},
month = {10}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 14 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Avian Visual Pigments: Characteristics, Spectral Tuning, and Evolution
journal, January 2007
- Hart, Nathan S.; Hunt, David M.
- The American Naturalist, Vol. 169, Issue S1
The cone oil droplets of avian retinas
journal, January 1984
- Goldsmith, Timothy H.; Collins, James S.; Licht, Sherry
- Vision Research, Vol. 24, Issue 11
Evolution and spectral tuning of visual pigments in birds and mammals
journal, October 2009
- Hunt, David M.; Carvalho, Livia S.; Cowing, Jill A.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 364, Issue 1531
Ultraviolet vision in birds: the importance of transparent eye media
journal, January 2014
- Lind, Olle; Mitkus, Mindaugas; Olsson, Peter
- Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1774
Evolution of Avian Plumage Color in a Tetrahedral Color Space: A Phylogenetic Analysis of New World Buntings
journal, June 2008
- Stoddard, Mary Caswell; Prum, Richard O.
- The American Naturalist, Vol. 171, Issue 6
Preprocessing strategies to improve MCR analyses of hyperspectral images
journal, August 2012
- Jones, Howland D.T.; Haaland, David M.; Sinclair, Michael B.
- Chemometrics and Intelligent Laboratory Systems, Vol. 117, p. 149-158
In search of the visual pigment template
journal, July 2000
- Govardovskii, Victor I.; Fyhrquist, Nanna; Reuter, Tom
- Visual Neuroscience, Vol. 17, Issue 4
Longitudinal chromatic aberration of the vertebrate eye
journal, January 1983
- Mandelman, T.; Sivak, J. G.
- Vision Research, Vol. 23, Issue 12
Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds
journal, August 1997
- Bowmaker, J. K.; Heath, L. A.; Wilkie, S. E.
- Vision Research, Vol. 37, Issue 16
Galloxanthin, a Carotenoid from the Chicken Retina
journal, May 1948
- Wald, G.
- The Journal of General Physiology, Vol. 31, Issue 5
In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells
journal, March 2008
- Vermaas, W. F. J.; Timlin, J. A.; Jones, H. D. T.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 10, p. 4050-4055
Oil droplets of bird eyes: microlenses acting as spectral filters
journal, February 2014
- Stavenga, Doekele G.; Wilts, Bodo D.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1636
Modified Saponification and HPLC Methods for Analyzing Carotenoids from the Retina of Quail: Implications for Its Use as a Nonprimate Model Species
journal, September 2007
- Toomey, Matthew B.; McGraw, Kevin J.
- Investigative Opthalmology & Visual Science, Vol. 48, Issue 9
Spectral tuning in vertebrate short wavelength-sensitive 1 (SWS1) visual pigments: Can wavelength sensitivity be inferred from sequence data?: SPECTRAL TUNING IN VERTEBRATE SWS1
journal, June 2014
- Hauser, Frances E.; van Hazel, Ilke; Chang, Belinda S. W.
- Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Vol. 322, Issue 7
Mate choice for a male carotenoid-based ornament is linked to female dietary carotenoid intake and accumulation
journal, January 2012
- Toomey, Matthew B.; McGraw, Kevin J.
- BMC Evolutionary Biology, Vol. 12, Issue 1
SWS2 visual pigment evolution as a test of historically contingent patterns of plumage color evolution in warblers: EVOLUTION OF SWS2 VISUAL PIGMENTS IN BIRDS
journal, January 2015
- Bloch, Natasha I.; Morrow, James M.; Chang, Belinda S. W.
- Evolution, Vol. 69, Issue 2
Optimization, Constraint, and History in the Evolution of Eyes
journal, September 1990
- Goldsmith, Timothy H.
- The Quarterly Review of Biology, Vol. 65, Issue 3, p. 281-322
Molecular evolution of vertebrate visual pigments
journal, July 2000
- Yokoyama, Shozo
- Progress in Retinal and Eye Research, Vol. 19, Issue 4
Coloured oil droplets enhance colour discrimination
journal, June 2003
- Vorobyev, M.
- Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 270, Issue 1521
A new method for determining peak absorbance of dense pigment samples and its application to the cone oil droplets ofEmydoidea blandingii
journal, January 1984
- Lipetz, Leo E.
- Vision Research, Vol. 24, Issue 6
Spectral sensitivity of the accessory optic system of the pigeon
journal, June 1998
- v. Campenhausen, M.; Kirschfeld, K.
- Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, Vol. 183, Issue 1
Comparing entire colour patterns as birds see them: COLOUR PATTERN DIFFERENCES
journal, November 2005
- Endler, John A.; Mielke, Paul W.
- Biological Journal of the Linnean Society, Vol. 86, Issue 4
Low aqueous solubility of 11-cis-retinal limits the rate of pigment formation and dark adaptation in salamander rods
journal, May 2012
- Frederiksen, Rikard; Boyer, Nicholas P.; Nickle, Benjamin
- The Journal of General Physiology, Vol. 139, Issue 6
Avian Cone Photoreceptors Tile the Retina as Five Independent, Self-Organizing Mosaics
journal, February 2010
- Kram, Yoseph A.; Mantey, Stephanie; Corbo, Joseph C.
- PLoS ONE, Vol. 5, Issue 2
Avian Color Vision and Coloration: Multidisciplinary Evolutionary Biology
journal, January 2007
- Bennett, Andrew T. D.; Théry, Marc
- The American Naturalist, Vol. 169, Issue S1
Avian retinal oil droplets: dietary manipulation of colour vision?
journal, November 2009
- Knott, Ben; Berg, Mathew L.; Morgan, Eric R.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 277, Issue 1683
The contribution of single and double cones to spectral sensitivity in budgerigars during changing light conditions
journal, December 2013
- Lind, Olle; Chavez, Johanna; Kelber, Almut
- Journal of Comparative Physiology A, Vol. 200, Issue 3
The Molecular Evolution of Avian Ultraviolet- and Violet-Sensitive Visual Pigments
journal, June 2007
- Carvalho, Livia S.; Cowing, Jill A.; Wilkie, Susan E.
- Molecular Biology and Evolution, Vol. 24, Issue 8
Carotenoids of the Chicken Retina
journal, July 1937
- Wald, George; Zussman, Hyman
- Nature, Vol. 140, Issue 3535
Silhouettes: A graphical aid to the interpretation and validation of cluster analysis
journal, November 1987
- Rousseeuw, Peter J.
- Journal of Computational and Applied Mathematics, Vol. 20
Multiple microscopic approaches demonstrate linkage between chromoplast architecture and carotenoid composition in diverse Capsicum annuum fruit
journal, November 2013
- Kilcrease, James; Collins, Aaron M.; Richins, Richard D.
- The Plant Journal, Vol. 76, Issue 6
Carotenoid metabolism in mammals, including man: formation, occurrence, and function of apocarotenoids: Thematic Review Series: Fat-Soluble Vitamins: Vitamin A
journal, May 2013
- Eroglu, Abdulkerim; Harrison, Earl H.
- Journal of Lipid Research, Vol. 54, Issue 7
Molecular evolution of color vision of zebra finch
journal, December 2000
- Yokoyama, Shozo; Blow, Nathan S.; Radlwimmer, F. Bernhard
- Gene, Vol. 259, Issue 1-2
Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity
journal, December 2006
- Hart, N. S.; Lisney, T. J.; Collin, S. P.
- Journal of Experimental Biology, Vol. 209, Issue 23
Evolution of ultraviolet vision in the largest avian radiation - the passerines
journal, January 2011
- Ödeen, Anders; Håstad, Olle; Alström, Per
- BMC Evolutionary Biology, Vol. 11, Issue 1
Multivariate curve resolution applied to second order data
journal, November 1995
- Tauler, Roma
- Chemometrics and Intelligent Laboratory Systems, Vol. 30, Issue 1
Simple exponential functions describing the absorbance bands of visual pigment spectra
journal, May 1993
- Stavenga, D. G.; Smits, R. P.; Hoenders, B. J.
- Vision Research, Vol. 33, Issue 8
Limited variation in visual sensitivity among bowerbird species suggests that there is no link between spectral tuning and variation in display colouration
journal, March 2012
- Coyle, B. J.; Hart, N. S.; Carleton, K. L.
- Journal of Experimental Biology, Vol. 215, Issue 7
The Visual Ecology of Avian Photoreceptors
journal, September 2001
- Hart, Nathan S.
- Progress in Retinal and Eye Research, Vol. 20, Issue 5
Tetrachromacy, oil droplets and bird plumage colours
journal, November 1998
- Vorobyev, M.; Osorio, D.; Bennett, A. T. D.
- Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, Vol. 183, Issue 5
Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors
journal, February 2005
- Hart, Nathan S.; Vorobyev, Misha
- Journal of Comparative Physiology A, Vol. 191, Issue 4
Excited State Properties of Peridinin: Observation of a Solvent Dependence of the Lowest Excited Singlet State Lifetime and Spectral Behavior Unique among Carotenoids
journal, October 1999
- Bautista, James A.; Connors, Robert E.; Raju, B. Bangar
- The Journal of Physical Chemistry B, Vol. 103, Issue 41
Super dense carotenoid spectra resolved in single cone oil droplets
journal, January 1975
- Liebman, P. A.; Granda, A. M.
- Nature, Vol. 253, Issue 5490
Functional characterization of spectral tuning mechanisms in the great bowerbird short-wavelength sensitive visual pigment (SWS1), and the origins of UV/violet vision in passerines and parrots
journal, January 2013
- van Hazel, Ilke; Sabouhanian, Amir; Day, Lainy
- BMC Evolutionary Biology, Vol. 13, Issue 1
Hyperspectral confocal microscope
journal, January 2006
- Sinclair, Michael B.; Haaland, David M.; Timlin, Jerilyn A.
- Applied Optics, Vol. 45, Issue 24, p. 6283-6291
Multivariate Curve Resolution in the Analysis of Vibrational Spectroscopy Data Files
journal, May 2003
- Schoonover, Jon R.; Marx, Rob; Zhang, Shuliang L.
- Applied Spectroscopy, Vol. 57, Issue 5
Fast algorithm for the solution of large-scale non-negativity-constrained least squares problems
journal, October 2004
- Van Benthem, Mark H.; Keenan, Michael R.
- Journal of Chemometrics, Vol. 18, Issue 10
Effect of carotenoid structure on excited-state dynamics of carbonyl carotenoids
journal, January 2009
- Chábera, Pavel; Fuciman, Marcel; Hříbek, Petr
- Physical Chemistry Chemical Physics, Vol. 11, Issue 39
The Effects of Dietary Carotenoid Supplementation and Retinal Carotenoid Accumulation on Vision-Mediated Foraging in the House Finch
journal, June 2011
- Toomey, Matthew B.; McGraw, Kevin J.
- PLoS ONE, Vol. 6, Issue 6
Works referencing / citing this record:
High-density lipoprotein receptor SCARB1 is required for carotenoid coloration in birds
journal, May 2017
- Toomey, Matthew B.; Lopes, Ricardo J.; Araújo, Pedro M.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 20
The effects of sun exposure on carotenoid accumulation and oxidative stress in the retina of the House Finch (Haemorhous mexicanus)
journal, March 2016
- Toomey, Matthew B.; McGraw, Kevin J.
- Avian Research, Vol. 7, Issue 1
Dietary carotenoid availability affects avian color discrimination
journal, July 2016
- Lim, Hui Hui; Pike, Thomas W.
- Behavioral Ecology
Light propagation and capture in cone photoreceptors
journal, January 2018
- Meadway, Alexander; Sincich, Lawrence C.
- Biomedical Optics Express, Vol. 9, Issue 11
Evolution, Development and Function of Vertebrate Cone Oil Droplets
journal, December 2017
- Toomey, Matthew B.; Corbo, Joseph C.
- Frontiers in Neural Circuits, Vol. 11
Evolution of CYP2J19, a gene involved in colour vision and red coloration in birds: positive selection in the face of conservation and pleiotropy
journal, February 2018
- Twyman, Hanlu; Andersson, Staffan; Mundy, Nicholas I.
- BMC Evolutionary Biology, Vol. 18, Issue 1
Coevolution of coloration and colour vision?
journal, May 2017
- Lind, Olle; Henze, Miriam J.; Kelber, Almut
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1724
Light propagation and capture in cone photoreceptors
journal, January 2018
- Meadway, Alexander; Sincich, Lawrence C.
- Biomedical Optics Express, Vol. 9, Issue 11
High-density lipoprotein receptor SCARB1 is required for carotenoid coloration in birds
journal, May 2017
- Toomey, Matthew B.; Lopes, Ricardo J.; Araújo, Pedro M.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 20
Coevolution of coloration and colour vision?
journal, May 2017
- Lind, Olle; Henze, Miriam J.; Kelber, Almut
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1724
Dietary carotenoid availability affects avian color discrimination
journal, July 2016
- Lim, Hui Hui; Pike, Thomas W.
- Behavioral Ecology
Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds
journal, July 2016
- Toomey, Matthew B.; Lind, Olle; Frederiksen, Rikard
- eLife, Vol. 5