Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds

Author:

Toomey Matthew B1ORCID,Lind Olle2,Frederiksen Rikard3,Curley Robert W4,Riedl Ken M56,Wilby David7ORCID,Schwartz Steven J5,Witt Christopher C89ORCID,Harrison Earl H10,Roberts Nicholas W7ORCID,Vorobyev Misha11,McGraw Kevin J12,Cornwall M Carter3,Kelber Almut13ORCID,Corbo Joseph C1ORCID

Affiliation:

1. Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, United States

2. Department of Philosophy, Lund University, Lund, Sweden

3. Department of Physiology and Biophysics, Boston University, Boston, United States

4. College of Pharmacy, The Ohio State University, Columbus, United States

5. Department of Food Science and Technology, The Ohio State University, Columbus, United States

6. Nutrient and Phytochemical Shared Resource of the OSU-Comprehensive Cancer Center, Columbus, United States

7. School of Biological Sciences, University of Bristol, Bristol, United Kingdom

8. Department of Biology, University of New Mexico, Albuquerque, United States

9. Museum of Southwestern Biology, University of New Mexico, Albuquerque, United States

10. Department of Human Nutrition, The Ohio State University, Columbus, United States

11. Department of Optometry and Vision Science, University of Auckland, Auckland, New Zealand

12. School of Life Sciences, Arizona State University, Tempe, United States

13. Department of Biology, Lund University, Lund, Sweden

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.

Funder

National Science Foundation

McDonnell Center for Cellular And Molecular Neurobiology

National Institutes of Health

Vetenskapsrådet

Air Force Office of Scientific Research

Engineering and Physical Sciences Research Council

Human Frontier Science Program

Knut och Alice Wallenbergs Stiftelse

Research to Prevent Blindness

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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