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Title: A complex carotenoid palette tunes avian color vision.

Journal Article · · Journal of the Royal Society Interface
 [1];  [2];  [3];  [4];  [4];  [2]
  1. Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
  2. Washington Univ. School of Medicine, St. Louis, MO (United States)
  3. Sandia National Lab. (SNL-NM), Albuquerque, NM (United States); Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  4. Boston Univ. School of Medicine, Boston, MA (United States)

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.

Research Organization:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
AC04-94AL85000
OSTI ID:
1236232
Report Number(s):
SAND-2015-4230J; 590324
Journal Information:
Journal of the Royal Society Interface, Vol. 12, Issue 111; ISSN 1742-5689
Publisher:
The Royal SocietyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 41 works
Citation information provided by
Web of Science

References (56)

Avian Visual Pigments: Characteristics, Spectral Tuning, and Evolution journal January 2007
Carotenoids of the Chicken Retina journal January 1938
The cone oil droplets of avian retinas journal January 1984
Evolution and spectral tuning of visual pigments in birds and mammals journal October 2009
Low aqueous solubility of 11-cis-retinal limits the rate of pigment formation and dark adaptation in salamander rods journal October 2014
Ultraviolet vision in birds: the importance of transparent eye media journal January 2014
Evolution of Avian Plumage Color in a Tetrahedral Color Space: A Phylogenetic Analysis of New World Buntings journal June 2008
Preprocessing strategies to improve MCR analyses of hyperspectral images journal August 2012
In search of the visual pigment template journal July 2000
Longitudinal chromatic aberration of the vertebrate eye journal January 1983
Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds journal August 1997
Galloxanthin, a Carotenoid from the Chicken Retina journal May 1948
In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells journal March 2008
Oil droplets of bird eyes: microlenses acting as spectral filters journal February 2014
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
Spectral tuning in vertebrate short wavelength-sensitive 1 (SWS1) visual pigments: Can wavelength sensitivity be inferred from sequence data?: SPECTRAL TUNING IN VERTEBRATE SWS1
  • Hauser, Frances E.; van Hazel, Ilke; Chang, Belinda S. W.
  • Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Vol. 322, Issue 7 https://doi.org/10.1002/jez.b.22576
journal June 2014
Mate choice for a male carotenoid-based ornament is linked to female dietary carotenoid intake and accumulation journal January 2012
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
Optimization, Constraint, and History in the Evolution of Eyes journal September 1990
Molecular evolution of vertebrate visual pigments journal July 2000
Coloured oil droplets enhance colour discrimination journal June 2003
A new method for determining peak absorbance of dense pigment samples and its application to the cone oil droplets ofEmydoidea blandingii journal January 1984
Spectral sensitivity of the accessory optic system of the pigeon journal June 1998
Comparing entire colour patterns as birds see them: COLOUR PATTERN DIFFERENCES journal November 2005
Low aqueous solubility of 11-cis-retinal limits the rate of pigment formation and dark adaptation in salamander rods journal May 2012
Avian Cone Photoreceptors Tile the Retina as Five Independent, Self-Organizing Mosaics journal February 2010
Avian Color Vision and Coloration: Multidisciplinary Evolutionary Biology journal January 2007
Avian retinal oil droplets: dietary manipulation of colour vision? journal November 2009
Towards clinically actionable digital phenotyping targets in schizophrenia journal May 2020
Avian Color Vision and Coloration: Multidisciplinary Evolutionary Biology journal January 2007
The contribution of single and double cones to spectral sensitivity in budgerigars during changing light conditions journal December 2013
The Molecular Evolution of Avian Ultraviolet- and Violet-Sensitive Visual Pigments journal June 2007
Carotenoids of the Chicken Retina journal July 1937
Silhouettes: A graphical aid to the interpretation and validation of cluster analysis journal November 1987
Multiple microscopic approaches demonstrate linkage between chromoplast architecture and carotenoid composition in diverse Capsicum annuum fruit journal November 2013
Carotenoid metabolism in mammals, including man: formation, occurrence, and function of apocarotenoids: Thematic Review Series: Fat-Soluble Vitamins: Vitamin A journal May 2013
Molecular evolution of color vision of zebra finch journal December 2000
Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity journal December 2006
Evolution of ultraviolet vision in the largest avian radiation - the passerines journal January 2011
Multivariate curve resolution applied to second order data journal November 1995
Simple exponential functions describing the absorbance bands of visual pigment spectra journal May 1993
The roles of receptor noise and cone oil droplets in the photopic spectral sensitivity of the budgerigar, Melopsittacus undulatus journal February 2003
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
The Visual Ecology of Avian Photoreceptors journal September 2001
Tetrachromacy, oil droplets and bird plumage colours journal November 1998
Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors journal February 2005
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
Super dense carotenoid spectra resolved in single cone oil droplets journal January 1975
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
Hyperspectral confocal microscope journal January 2006
Multivariate Curve Resolution in the Analysis of Vibrational Spectroscopy Data Files journal May 2003
Fast algorithm for the solution of large-scale non-negativity-constrained least squares problems journal October 2004
SWS2 visual pigment evolution as a test of historically contingent patterns of plumage color evolution in Warblers posted_content January 2015
Effect of carotenoid structure on excited-state dynamics of carbonyl carotenoids journal January 2009
The Effects of Dietary Carotenoid Supplementation and Retinal Carotenoid Accumulation on Vision-Mediated Foraging in the House Finch journal June 2011
Colour vision of domestic chicks journal November 1999

Cited By (17)

High-density lipoprotein receptor SCARB1 is required for carotenoid coloration in birds journal May 2017
The effects of sun exposure on carotenoid accumulation and oxidative stress in the retina of the House Finch (Haemorhous mexicanus) journal March 2016
Body coloration and mechanisms of colour production in Archelosauria: the case of deirocheline turtles journal July 2019
Light propagation and capture in cone photoreceptors journal January 2018
Evolution, Development and Function of Vertebrate Cone Oil Droplets journal December 2017
Carotenoid composition and conformation in retinal oil droplets of the domestic chicken* journal May 2019
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
Coevolution of coloration and colour vision? journal May 2017
Simple and complex retinal dystrophies are associated with profoundly different disease networks journal January 2017
Colour vision and background adaptation in a passerine bird, the zebra finch ( Taeniopygia guttata ) journal September 2016
Structure versus time in the evolutionary diversification of avian carotenoid metabolic networks journal March 2018
Evolution of CYP2J19, a gene involved in colour vision and red coloration in birds: positive selection in the face of conservation and pleiotropy. text January 2018
Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds journal July 2016
Convergent evolution of cytochrome P450s underlies independent origins of keto-carotenoid pigmentation in animals journal July 2019
Optical influence of oil droplets on cone photoreceptor sensitivity journal January 2017
Dietary carotenoid availability affects avian color discrimination journal July 2016
Body coloration and mechanisms of colour production in Archelosauria: The case of deirocheline turtles journal February 2019