title: Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds.
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.
authors.affiliation: Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, United States.
authors.forename: Matthew B
authors.identifier: 0000-0001-9184-197X
authors.initials: MB
authors.lastname: Toomey
authors.affiliation: Department of Philosophy, Lund University, Lund, Sweden.
authors.forename: Olle
authors.initials: O
authors.lastname: Lind
authors.affiliation: Department of Physiology and Biophysics, Boston University, Boston, United States.
authors.forename: Rikard
authors.initials: R
authors.lastname: Frederiksen
authors.affiliation: College of Pharmacy, The Ohio State University, Columbus, United States.
authors.forename: Robert W
authors.initials: RW
authors.lastname: Curley
authors.affiliation: Department 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 States.
authors.forename: Ken M
authors.initials: KM
authors.lastname: Riedl
authors.affiliation: School of Biological Sciences, University of Bristol, Bristol, United Kingdom.
authors.forename: David
authors.identifier: 0000-0002-6553-8739
authors.initials: D
authors.lastname: Wilby
authors.affiliation: Department of Food Science and Technology, The Ohio State University, Columbus, United States.
authors.forename: Steven J
authors.initials: SJ
authors.lastname: Schwartz
authors.affiliation: Department of Biology, University of New Mexico, Albuquerque, United States.|Museum of Southwestern Biology, University of New Mexico, Albuquerque, United States.
authors.forename: Christopher C
authors.identifier: 0000-0003-2781-1543
authors.initials: CC
authors.lastname: Witt
authors.affiliation: Department of Human Nutrition, The Ohio State University, Columbus, United States.
authors.forename: Earl H
authors.initials: EH
authors.lastname: Harrison
authors.affiliation: School of Biological Sciences, University of Bristol, Bristol, United Kingdom.
authors.forename: Nicholas W
authors.identifier: 0000-0002-4540-6683
authors.initials: NW
authors.lastname: Roberts
authors.affiliation: Department of Optometry and Vision Science, University of Auckland, Auckland, New Zealand.
authors.forename: Misha
authors.initials: M
authors.lastname: Vorobyev
authors.affiliation: School of Life Sciences, Arizona State University, Tempe, United States.
authors.forename: Kevin J
authors.initials: KJ
authors.lastname: McGraw
authors.affiliation: Department of Physiology and Biophysics, Boston University, Boston, United States.
authors.forename: M Carter
authors.initials: MC
authors.lastname: Cornwall
authors.affiliation: Department of Biology, Lund University, Lund, Sweden.
authors.forename: Almut
authors.identifier: 0000-0003-3937-2808
authors.initials: A
authors.lastname: Kelber
authors.affiliation: Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, United States.
authors.forename: Joseph C
authors.identifier: 0000-0002-9323-7140
authors.initials: JC
authors.lastname: Corbo
mesh_terms: D000818:Animals; D005075:Biological Evolution; D001717:Birds / Q000502:physiology*; D002338:Carotenoids / Q000378:metabolism*; D017949:Retinal Cone Photoreceptor Cells / Q000737:chemistry* / Q000502:physiology* / Q000528:radiation effects; D014466:Ultraviolet Rays; D014785:Vision, Ocular
chemical_list: C000609456:galloxanthin; D002338:Carotenoids
keywords: biochemistry; birds; carotenoids; chicken; neuroscience; photoreceptors; retina; sensory ecology; spectral tuning