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

Toomey, Matthew B.; Lind, Olle LU ; Frederiksen, Rikard LU ; Curley, Robert W.; Riedl, Ken M.; Wilby, David LU ; Schwartz, Steven J.; Witt, Christopher C.; Harrison, Earl H. and Roberts, Nicholas W., et al. (2016) In eLife 5.
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... (More)

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.

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eLife
volume
5
publisher
eLife Sciences Publications LTD.
external identifiers
  • scopus:84979502825
  • wos:000380852700001
ISSN
2050-084X
DOI
10.7554/eLife.15675
language
English
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yes
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a8082740-5da6-48da-a9eb-55708d660a79
date added to LUP
2016-10-05 10:34:48
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2017-04-16 04:40:41
@article{a8082740-5da6-48da-a9eb-55708d660a79,
  abstract     = {<p>Color vision in birds is mediated by four types of cone photoreceptors whose maximal sensitivities (λ<sub>max</sub>) are evenly spaced across the light spectrum. In the course of avian evolution, the λ<sub>max</sub> of the most shortwave-sensitive cone, SWS1, has switched between violet (λ<sub>max</sub> &gt; 400 nm) and ultraviolet (λ<sub>max</sub> &lt; 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.</p>},
  articleno    = {e15675},
  author       = {Toomey, Matthew B. and Lind, Olle and Frederiksen, Rikard and Curley, Robert W. and Riedl, Ken M. and Wilby, David and Schwartz, Steven J. and Witt, Christopher C. and Harrison, Earl H. and Roberts, Nicholas W. and Vorobyev, Misha and McGraw, Kevin J. and Cornwall, M. Carter and Kelber, Almut and Corbo, Joseph C.},
  issn         = {2050-084X},
  language     = {eng},
  month        = {07},
  publisher    = {eLife Sciences Publications LTD.},
  series       = {eLife},
  title        = {Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds},
  url          = {http://dx.doi.org/10.7554/eLife.15675},
  volume       = {5},
  year         = {2016},
}