title: Evolutionary transformation of rod photoreceptors in the all-cone retina of a diurnal garter snake.
abstract: Vertebrate retinas are generally composed of rod (dim-light) and cone (bright-light) photoreceptors with distinct morphologies that evolved as adaptations to nocturnal/crepuscular and diurnal light environments. Over 70 years ago, the "transmutation" theory was proposed to explain some of the rare exceptions in which a photoreceptor type is missing, suggesting that photoreceptors could evolutionarily transition between cell types. Although studies have shown support for this theory in nocturnal geckos, the origins of all-cone retinas, such as those found in diurnal colubrid snakes, remain a mystery. Here we investigate the evolutionary fate of the rods in a diurnal garter snake and test two competing hypotheses: (i) that the rods, and their corresponding molecular machinery, were lost or (ii) that the rods were evolutionarily modified to resemble, and function, as cones. Using multiple approaches, we find evidence for a functional and unusually blue-shifted rhodopsin that is expressed in small single "cones." Moreover, these cones express rod transducin and have rod ultrastructural features, providing strong support for the hypothesis that they are not true cones, as previously thought, but rather are modified rods. Several intriguing features of garter snake rhodopsin are suggestive of a more cone-like function. We propose that these cone-like rods may have evolved to regain spectral sensitivity and chromatic discrimination as a result of ancestral losses of middle-wavelength cone opsins in early snake evolution. This study illustrates how sensory evolution can be shaped not only by environmental constraints but also by historical contingency in forming new cell types with convergent functionality.
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Ryan K
authors.initials: RK
authors.lastname: Schott
authors.affiliation: Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, 10115 Berlin, Germany;
authors.forename: Johannes
authors.initials: J
authors.lastname: Müller
authors.affiliation: Department of Cell & Systems Biology, University of Toronto, Toronto, ON, Canada M5S 3G5;
authors.forename: Clement G Y
authors.initials: CG
authors.lastname: Yang
authors.affiliation: Department of Cell & Systems Biology, University of Toronto, Toronto, ON, Canada M5S 3G5;
authors.forename: Nihar
authors.initials: N
authors.lastname: Bhattacharyya
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Natalie
authors.initials: N
authors.lastname: Chan
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Mengshu
authors.initials: M
authors.lastname: Xu
authors.affiliation: Department of Cell & Systems Biology, University of Toronto, Toronto, ON, Canada M5S 3G5;
authors.forename: James M
authors.initials: JM
authors.lastname: Morrow
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Ana-Hermina
authors.initials: AH
authors.lastname: Ghenu
authors.affiliation: Department of Biomedical Sciences, Cornell University, Ithaca, NY 14853-6401;
authors.forename: Ellis R
authors.initials: ER
authors.lastname: Loew
authors.affiliation: Department of Cell & Systems Biology, University of Toronto, Toronto, ON, Canada M5S 3G5; Department of Ophthalmology & Vision Sciences, University of Toronto, Toronto ON, Canada M5T 3A9; Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, ON, Canada M5S 3B2.
authors.forename: Vincent
authors.initials: V
authors.lastname: Tropepe
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2; Department of Cell & Systems Biology, University of Toronto, Toronto, ON, Canada M5S 3G5; Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, ON, Canada M5S 3B2 belinda.chang@utoronto.ca.
authors.forename: Belinda S W
authors.initials: BS
authors.lastname: Chang
mesh_terms: D000818:Animals; D005075:Biological Evolution; D002940:Circadian Rhythm; D017812:Colubridae / Q000502:physiology*; D007150:Immunohistochemistry; D051379:Mice; D008954:Models, Biological; D008969:Molecular Sequence Data; D017949:Retinal Cone Photoreceptor Cells / Q000166:cytology* / Q000648:ultrastructure; D012168:Retinal Pigments / Q000378:metabolism; D017948:Retinal Rod Photoreceptor Cells / Q000166:cytology / Q000648:ultrastructure; D012243:Rhodopsin / Q000378:metabolism; D015293:Transducin / Q000378:metabolism
chemical_list: D012168:Retinal Pigments; D012243:Rhodopsin; D015293:Transducin
keywords: reptile vision; rhodopsin evolution; snake photoreceptors; visual evolution; visual pigment