imultaneous Expression of UV and Violet SWS1 Opsins Expands the Visual Palette in a Group of Freshwater Snake

Author(s)

Hauzman, Einat ^{[1, 2]} ; Pierotti, Michele E. R. ^[3] ; Bhattacharyya, Nihar ^[4] ; Tashiro, Juliana H. ^[2] ; Yovanovich, Carola A. M. ^{[3, 5]} ; Campos, Pollyanna F. ^[6] ; Ventura, Dora F. ^{[1, 2]} ; Chang, Belinda S. W. ^{[7, 4]}

Affiliation

^[1] Hosp Israelita Albert Einstein, Sao Paulo - Brazil

^[2] Univ Sao Paulo, Psychol Inst, Dept Expt Psychol, Sao Paulo - Brazil

^[3] Univ Sao Paulo, Inst Biosci, Dept Zool, Sao Paulo - Brazil

^[4] Univ Toronto, Dept Cell & Syst Biol, Toronto, ON - Canada

^[5] Univ Sussex, Sch Life Sci, Brighton, E Sussex - England

^[6] Inst Butantan, Ctr Toxins Immune Response & Cell Signaling CeTIC, Lab Toxinol Aplicada, Sao Paulo - Brazil

^[7] Univ Toronto, Dept Ecol & Evolutionary Biol, Toronto, ON - Canada

• Document type: Journal article
• Source: Molecular Biology and Evolution; v. 38, n. 12, p. 5225-5240, DEC 2021.
• Web of Science Citations: 0

Abstract

Snakes are known to express a rod visual opsin and two cone opsins, only (SWS1, LWS), a reduced palette resulting from their supposedly fossorial origins. Dipsadid snakes in the genus Helicops are highly visual predators that successfully invaded freshwater habitats from ancestral terrestrial-only habitats. Here, we report the first case of multiple SWS1 visual pigments in a vertebrate, simultaneously expressed in different photoreceptors and conferring both UV and violet sensitivity to Helicops snakes. Molecular analysis and in vitro expression confirmed the presence of two functional SWS1 opsins, likely the result of recent gene duplication. Evolutionary analyses indicate that each swsl variant has undergone different evolutionary paths with strong purifying selection acting on the UV-sensitive copy and d(N)/d(S) similar to 1 on the violet-sensitive copy. Site-directed mutagenesis points to the functional role of a single amino acid substitution, Phe86Val, in the large spectral shift between UV and violet opsins. In addition, higher densities of photoreceptors and SWS1 cones in the ventral retina suggest improved acuity in the upper visual field possibly correlated with visually guided behaviors. The expanded visual opsin repertoire and specialized retinal architecture are likely to improve photon uptake in underwater and terrestrial environments, and provide the neural substrate for a gain in chromatic discrimination, potentially conferring unique color vision in the UV-violet range. Our findings highlight the innovative solutions undertaken by a highly specialized lineage to tackle the challenges imposed by the invasion of novel photic environments and the extraordinary diversity of evolutionary trajectories taken by visual opsin-based perception in vertebrates. (AU)

• FAPESP's process: 18/11502-0 - The hyperdiverse amphibian fauna of Brazil as a model system for comparative ecophysiology and genomics of vision
• Grantee: Taran Grant
• Support Opportunities: Research Grants - Visiting Researcher Grant - International
• FAPESP's process: 14/26818-2 - Development and implementation of visual evaluation methods: clinical applications and animal models
• Grantee: Dora Selma Fix Ventura
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 18/13910-9 - Comparative studies of retinal morphology of Bothrops jararaca and Crotalus durissus terrificus (Serpentes, Viperidae): density and topography of photoreceptors and ganglion cell, and estimation of visual acuity
• Grantee: Juliana Hiromi Tashiro
• Support Opportunities: Scholarships in Brazil - Master
• FAPESP's process: 14/25743-9 - Expression of opsins and melanopsins in snakes' retinas: molecular genetics and immunohistochemistry
• Grantee: Einat Hauzman
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 18/09321-8 - In vitro expression and spectral absorption measurements of the SWS1 photopigment of the Colubridae snake Helicops modestus
• Grantee: Einat Hauzman
• Support Opportunities: Scholarships abroad - Research Internship - Post-doctor
• FAPESP's process: 13/07467-1 - CeTICS - Center of Toxins, Immune-Response and Cell Signaling
• Grantee: Hugo Aguirre Armelin
• Support Opportunities: Research Grants - Research, Innovation and Dissemination Centers - RIDC
• FAPESP's process: 15/14857-6 - A systematic study of amphibian visual systems: from evolution of diel patterns to physiological limits for colour vision
• Grantee: Carola Anabel Mariana Yovanovich
• Support Opportunities: Scholarships in Brazil - Post-Doctoral