Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds
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 ultravi...
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doaj-2cf4a36adec642dd836eef7ce69591f32021-05-05T00:28:36ZengeLife Sciences Publications LtdeLife2050-084X2016-07-01510.7554/eLife.15675Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birdsMatthew B Toomey0https://orcid.org/0000-0001-9184-197XOlle Lind1Rikard Frederiksen2Robert W Curley Jr3Ken M Riedl4David Wilby5https://orcid.org/0000-0002-6553-8739Steven J Schwartz6Christopher C Witt7https://orcid.org/0000-0003-2781-1543Earl H Harrison8Nicholas W Roberts9https://orcid.org/0000-0002-4540-6683Misha Vorobyev10Kevin J McGraw11M Carter Cornwall12Almut Kelber13https://orcid.org/0000-0003-3937-2808Joseph C Corbo14https://orcid.org/0000-0002-9323-7140Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, United StatesDepartment of Philosophy, Lund University, Lund, SwedenDepartment of Physiology and Biophysics, Boston University, Boston, United StatesCollege of Pharmacy, The Ohio State University, Columbus, United StatesDepartment of Food Science and Technology, The Ohio State University, Columbus, United States; Nutrient and Phytochemical Shared Resource of the OSU-Comprehensive Cancer Center, Columbus, United StatesSchool of Biological Sciences, University of Bristol, Bristol, United KingdomDepartment of Food Science and Technology, The Ohio State University, Columbus, United StatesDepartment of Biology, University of New Mexico, Albuquerque, United States; Museum of Southwestern Biology, University of New Mexico, Albuquerque, United StatesDepartment of Human Nutrition, The Ohio State University, Columbus, United StatesSchool of Biological Sciences, University of Bristol, Bristol, United KingdomDepartment of Optometry and Vision Science, University of Auckland, Auckland, New ZealandSchool of Life Sciences, Arizona State University, Tempe, United StatesDepartment of Physiology and Biophysics, Boston University, Boston, United StatesDepartment of Biology, Lund University, Lund, SwedenDepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, United StatesColor 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.https://elifesciences.org/articles/15675spectral tuningcarotenoidssensory ecologybirdsretinaphotoreceptors |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
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 Joseph C Corbo |
spellingShingle |
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 Joseph C Corbo Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds eLife spectral tuning carotenoids sensory ecology birds retina photoreceptors |
author_facet |
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 Joseph C Corbo |
author_sort |
Matthew B Toomey |
title |
Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds |
title_short |
Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds |
title_full |
Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds |
title_fullStr |
Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds |
title_full_unstemmed |
Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds |
title_sort |
complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2016-07-01 |
description |
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. |
topic |
spectral tuning carotenoids sensory ecology birds retina photoreceptors |
url |
https://elifesciences.org/articles/15675 |
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