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Cone-like rhodopsin expressed in the all cone retina of the colubrid pine snake as a potential adaptation to diurnality

Nihar Bhattacharyya, Benedict Darren, Ryan K. Schott, Vincent Tropepe, View ORCID ProfileBelinda S.W. Chang
doi: https://doi.org/10.1101/100792
Nihar Bhattacharyya
1Department of Cell & Systems Biology, University of Toronto, Toronto, Ontario, Canada
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Benedict Darren
1Department of Cell & Systems Biology, University of Toronto, Toronto, Ontario, Canada
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Ryan K. Schott
2Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada
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Vincent Tropepe
1Department of Cell & Systems Biology, University of Toronto, Toronto, Ontario, Canada
3Department of Ophthalmology & Vision Sciences, University of Toronto, Toronto ON, Canada M5T 3A9
4Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, Ontario, Canada
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Belinda S.W. Chang
1Department of Cell & Systems Biology, University of Toronto, Toronto, Ontario, Canada
2Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada
4Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, Ontario, Canada
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  • ORCID record for Belinda S.W. Chang
  • For correspondence: belinda.chang@utoronto.ca
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Abstract

Colubridae is the largest and most diverse family of snakes, with visual systems that reflect this diversity, encompassing a variety of retinal photoreceptor organizations. The transmutation theory proposed by Walls postulates that photoreceptors could evolutionarily transition between cell types in squamates, but few studies have tested this theory. Recently, evidence for transmutation and rod-like machinery in an all cone retina has been identified in a diurnal garter snake (Thamnophis), and it appears that the rhodopsin gene at least may be widespread among colubrid snakes. However, functional evidence supporting transmutation beyond the existence of the rhodopsin gene remains rare. We examined the all cone retina of another diurnal colubrid, Pituophis melanoleucus, distantly related to Thamnophis. We found that P. melanoleucus expresses two cone opsins (SWS1, LWS) and rhodopsin (RH1) within the eye. Immunohistochemistry localized rhodopsin to the outer segment of photoreceptors in the all-cone retina of the snake and all opsin genes produced functional visual pigments when expressed in vitro. Consistent with other studies, we found that P. melanoleucus rhodopsin is extremely blue-shifted. Surprisingly, P. melanoleucus rhodopsin reacted with hydroxylamine, a typical cone opsin characteristic. These results support the idea that the rhodopsin-containing photoreceptors of P. melanoleucus are the products of evolutionary transmutation from rod ancestors, and suggests that this phenomenon may be widespread in colubrid snakes. We hypothesize that transmutation may be an adaptation for diurnal, brighter-light vision, which could result in increased spectral sensitivity and chromatic discrimination with the potential for colour vision.

Summary Statement The all cone retina of the colubrid snake, Pituophis melanoleucus contains a blue-shifted rhodopsin with cone opsin-like properties, which may have been adaptive in diurnal snakes.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 18, 2017.
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Cone-like rhodopsin expressed in the all cone retina of the colubrid pine snake as a potential adaptation to diurnality
Nihar Bhattacharyya, Benedict Darren, Ryan K. Schott, Vincent Tropepe, Belinda S.W. Chang
bioRxiv 100792; doi: https://doi.org/10.1101/100792
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Cone-like rhodopsin expressed in the all cone retina of the colubrid pine snake as a potential adaptation to diurnality
Nihar Bhattacharyya, Benedict Darren, Ryan K. Schott, Vincent Tropepe, Belinda S.W. Chang
bioRxiv 100792; doi: https://doi.org/10.1101/100792

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