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The evolution of red color vision is linked to coordinated rhodopsin tuning in lycaenid butterflies

Liénard, Marjorie A. LU ; Bernard, Gary D. ; Allen, Andrew ; Lassance, Jean Marc LU ; Song, Siliang ; Childers, Richard Rabideau ; Yu, Nanfang ; Ye, Dajia ; Stephenson, Adriana and Valencia-Montoya, Wendy A. , et al. (2021) In Proceedings of the National Academy of Sciences of the United States of America 118(6).
Abstract

Color vision has evolved multiple times in both vertebrates and invertebrates and is largely determined by the number and variation in spectral sensitivities of distinct opsin subclasses. However, because of the difficulty of expressing long-wavelength (LW) invertebrate opsins in vitro, our understanding of the molecular basis of functional shifts in opsin spectral sensitivities has been biased toward research primarily in vertebrates. This has restricted our ability to address whether invertebrate Gq protein-coupled opsins function in a novel or convergent way compared to vertebrate Gt opsins. Here we develop a robust heterologous expression system to purify invertebrate rhodopsins, identify specific amino acid... (More)

Color vision has evolved multiple times in both vertebrates and invertebrates and is largely determined by the number and variation in spectral sensitivities of distinct opsin subclasses. However, because of the difficulty of expressing long-wavelength (LW) invertebrate opsins in vitro, our understanding of the molecular basis of functional shifts in opsin spectral sensitivities has been biased toward research primarily in vertebrates. This has restricted our ability to address whether invertebrate Gq protein-coupled opsins function in a novel or convergent way compared to vertebrate Gt opsins. Here we develop a robust heterologous expression system to purify invertebrate rhodopsins, identify specific amino acid changes responsible for adaptive spectral tuning, and pinpoint how molecular variation in invertebrate opsins underlie wavelength sensitivity shifts that enhance visual perception. By combining functional and optophysiological approaches, we disentangle the relative contributions of lateral filtering pigments from red-shifted LW and blue short-wavelength opsins expressed in distinct photoreceptor cells of individual ommatidia. We use in situ hybridization to visualize six ommatidial classes in the compound eye of a lycaenid butterfly with a four-opsin visual system. We show experimentally that certain key tuning residues underlying green spectral shifts in blue opsin paralogs have evolved repeatedly among short-wavelength opsin lineages. Taken together, our results demonstrate the interplay between regulatory and adaptive evolution at multiple Gq opsin loci, as well as how coordinated spectral shifts in LW and blue opsins can act together to enhance insect spectral sensitivity at blue and red wavelengths for visual performance adaptation.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Ecological adaptation, Insects, Molecular evolution, Spectral sensitivity, Visual system
in
Proceedings of the National Academy of Sciences of the United States of America
volume
118
issue
6
article number
e2008986118
publisher
National Acad Sciences
external identifiers
  • pmid:33547236
  • scopus:85100665580
ISSN
0027-8424
DOI
10.1073/pnas.2008986118
language
English
LU publication?
yes
id
ec006976-8f84-4804-ae7c-abb410b4850c
date added to LUP
2021-02-23 09:04:47
date last changed
2021-02-24 03:00:03
@article{ec006976-8f84-4804-ae7c-abb410b4850c,
  abstract     = {<p>Color vision has evolved multiple times in both vertebrates and invertebrates and is largely determined by the number and variation in spectral sensitivities of distinct opsin subclasses. However, because of the difficulty of expressing long-wavelength (LW) invertebrate opsins in vitro, our understanding of the molecular basis of functional shifts in opsin spectral sensitivities has been biased toward research primarily in vertebrates. This has restricted our ability to address whether invertebrate G<sub>q</sub> protein-coupled opsins function in a novel or convergent way compared to vertebrate G<sub>t</sub> opsins. Here we develop a robust heterologous expression system to purify invertebrate rhodopsins, identify specific amino acid changes responsible for adaptive spectral tuning, and pinpoint how molecular variation in invertebrate opsins underlie wavelength sensitivity shifts that enhance visual perception. By combining functional and optophysiological approaches, we disentangle the relative contributions of lateral filtering pigments from red-shifted LW and blue short-wavelength opsins expressed in distinct photoreceptor cells of individual ommatidia. We use in situ hybridization to visualize six ommatidial classes in the compound eye of a lycaenid butterfly with a four-opsin visual system. We show experimentally that certain key tuning residues underlying green spectral shifts in blue opsin paralogs have evolved repeatedly among short-wavelength opsin lineages. Taken together, our results demonstrate the interplay between regulatory and adaptive evolution at multiple G<sub>q</sub> opsin loci, as well as how coordinated spectral shifts in LW and blue opsins can act together to enhance insect spectral sensitivity at blue and red wavelengths for visual performance adaptation.</p>},
  author       = {Liénard, Marjorie A. and Bernard, Gary D. and Allen, Andrew and Lassance, Jean Marc and Song, Siliang and Childers, Richard Rabideau and Yu, Nanfang and Ye, Dajia and Stephenson, Adriana and Valencia-Montoya, Wendy A. and Salzman, Shayla and Whitaker, Melissa R.L. and Calonje, Michael and Zhang, Feng and Pierce, Naomi E.},
  issn         = {0027-8424},
  language     = {eng},
  number       = {6},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences of the United States of America},
  title        = {The evolution of red color vision is linked to coordinated rhodopsin tuning in lycaenid butterflies},
  url          = {http://dx.doi.org/10.1073/pnas.2008986118},
  doi          = {10.1073/pnas.2008986118},
  volume       = {118},
  year         = {2021},
}