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An EvoDevo Study of Salmonid Visual Opsin Dynamics and Photopigment Spectral Sensitivity
Department of Biological Sciences, University of Bergen, Bergen, Norway.
Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). School of Life Sciences, College of Science, Health and Engineering, La Trobe University, VIC, Melbourne, Australia.ORCID iD: 0000-0003-0232-1812
Institute for Modeling Collaboration and Innovation (IMCI), University of Idaho, ID, Moscow, United States.
Institute for Modeling Collaboration and Innovation (IMCI), University of Idaho, ID, Moscow, United States.
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2022 (English)In: Frontiers in Neuroanatomy, E-ISSN 1662-5129, Vol. 16, article id 945344Article in journal (Refereed) Published
Abstract [en]

Salmonids are ideal models as many species follow a distinct developmental program from demersal eggs and a large yolk sac to hatching at an advanced developmental stage. Further, these economically important teleosts inhabit both marine- and freshwaters and experience diverse light environments during their life histories. At a genome level, salmonids have undergone a salmonid-specific fourth whole genome duplication event (Ss4R) compared to other teleosts that are already more genetically diverse compared to many non-teleost vertebrates. Thus, salmonids display phenotypically plastic visual systems that appear to be closely related to their anadromous migration patterns. This is most likely due to a complex interplay between their larger, more gene-rich genomes and broad spectrally enriched habitats; however, the molecular basis and functional consequences for such diversity is not fully understood. This study used advances in genome sequencing to identify the repertoire and genome organization of visual opsin genes (those primarily expressed in retinal photoreceptors) from six different salmonids [Atlantic salmon (Salmo salar), brown trout (Salmo trutta), Chinook salmon (Oncorhynchus tshawytcha), coho salmon (Oncorhynchus kisutch), rainbow trout (Oncorhynchus mykiss), and sockeye salmon (Oncorhynchus nerka)] compared to the northern pike (Esox lucius), a closely related non-salmonid species. Results identified multiple orthologues for all five visual opsin classes, except for presence of a single short-wavelength-sensitive-2 opsin gene. Several visual opsin genes were not retained after the Ss4R duplication event, which is consistent with the concept of salmonid rediploidization. Developmentally, transcriptomic analyzes of Atlantic salmon revealed differential expression within each opsin class, with two of the long-wavelength-sensitive opsins not being expressed before first feeding. Also, early opsin expression in the retina was located centrally, expanding dorsally and ventrally as eye development progressed, with rod opsin being the dominant visual opsin post-hatching. Modeling by spectral tuning analysis and atomistic molecular simulation, predicted the greatest variation in the spectral peak of absorbance to be within the Rh2 class, with a ∼40 nm difference in λmax values between the four medium-wavelength-sensitive photopigments. Overall, it appears that opsin duplication and expression, and their respective spectral tuning profiles, evolved to maximize specialist color vision throughout an anadromous lifecycle, with some visual opsin genes being lost to tailor marine-based vision.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2022. Vol. 16, article id 945344
Keywords [en]
atomistic molecular simulation, eye, photoreception, RNA in situ hybridization, RNA sequencing, salmonid, visual opsin
National Category
Zoology Evolutionary Biology
Identifiers
URN: urn:nbn:se:umu:diva-198333DOI: 10.3389/fnana.2022.945344ISI: 000832800900001Scopus ID: 2-s2.0-85134699424OAI: oai:DiVA.org:umu-198333DiVA, id: diva2:1685284
Funder
The Research Council of Norway, 254894The Research Council of Norway, 315106NIH (National Institutes of Health), P30 GM103324Available from: 2022-08-02 Created: 2022-08-02 Last updated: 2024-01-15Bibliographically approved

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Davies, Wayne Iwan Lee

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