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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 λ max 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.
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A homology guide for Pacific salmon genus Oncorhynchus resolves patterns of ohnolog retention, resolution and local adaptation following the salmonid‐specific whole‐genome duplication event
Abstract Salmonid fishes have emerged as a tractable model to study whole‐genome duplications (WGDs) as this group has undergone four rounds of WGDs. While most of the salmonid genome has returned to a diploid state, a significant proportion of genes are maintained as duplicates and are referred to as ohnologs. The fact that much of the modern salmonid gene repertoire is comprised of ohnologs, while other genes have returned to their singleton state creates complications for genetic studies by obscuring homology relationships. The difficulty this creates is particularly prominent in Pacific salmonids belonging to genusOncorhynchuswho are the focus of intense genetics‐based conservation and management efforts owing to the important ecological and cultural roles these fish play. To address this gap, we generated a homology guide for six species ofOncorhynchuswith available genomes and used this guide to describe patterns of ohnolog retention and resolution. Overall, we find that ohnologs comprise approximately half of each species modern gene repertoires, which are functionally enriched for genes involved in DNA binding, while the less numerous singleton genes are heavily enriched in dosage‐sensitive processes such as mitochondrial metabolism. Additionally, by reanalyzing published expression data from locally adapted strains ofO. mykiss, we show that numerous ohnologs exhibit adaptive expression profiles; however, ohnologs are not more likely to display adaptive signatures than either paralogs or singletons. Finally, we demonstrate the utility of our homology guide by investigating the evolutionary relationship among genes highlighted as playing a role in salmonid life‐history traits or gene editing targets.
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- Award ID(s):
- 2109355
- PAR ID:
- 10419032
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 13
- Issue:
- 4
- ISSN:
- 2045-7758
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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