The Grayling Genome Reveals Selection on Gene Expression Regulation after Whole-Genome Duplication

Abstract

Whole-genome duplication (WGD) has been a major evolutionary driver of increased genomic complexity in vertebrates. One such event occurred in the salmonid family ∼80 Ma (Ss4R) giving rise to a plethora of structural and regulatory duplicate-driven divergence, making salmonids an exemplary system to investigate the evolutionary consequences of WGD. Here, we present a draft genome assembly of European grayling (Thymallus thymallus) and use this in a comparative framework to study evolution of gene regulation following WGD. Among the Ss4R duplicates identified in European grayling and Atlantic salmon (Salmo salar), one-third reflect nonneutral tissue expression evolution, with strong purifying selection, maintained over ∼50 Myr. Of these, the majority reflect conserved tissue regulation under strong selective constraints related to brain and neural-related functions, as well as higher-order protein–protein interactions. A small subset of the duplicates have evolved tissue regulatory expression divergence in a common ancestor, which have been subsequently conserved in both lineages, suggestive of adaptive divergence following WGD. These candidates for adaptive tissue expression divergence have elevated rates of protein coding- and promoter-sequence evolution and are enriched for immune- and lipid metabolism ontology terms. Lastly, lineage-specific duplicate divergence points toward underlying differences in adaptive pressures on expression regulation in the nonanadromous grayling versus the anadromous Atlantic salmon. Our findings enhance our understanding of the role of WGD in genome evolution and highlight cases of regulatory divergence of Ss4R duplicates, possibly related to a niche shift in early salmonid evolution.

Atlantic salmon (Salmo salar L.) genetics in the 21st century: taking leaps forward in aquaculture and biological understanding

“…), European grayling ( Thymallus thymallus ; Varadharajan et al . ) and Arctic charr ( Salvelinus alpinus ; Christensen et al . ), or are available yet currently unpublished, including for coho salmon ( Oncorhynchus kisutch ; NCBI accession no.…”

Extensive genetic differentiation between recently evolved sympatric Arctic charr morphs

“…Relatively few genomic resources have been available for Arctic charr, until recently when a reference genome was published (Christensen, Rondeau, Minkley, Leong, Nugent, Danzmann, Ferguson, Stadnik, Devlin, Muzzerall, Edwards, Davidson and Koop 2018). Reference genomes for other salmonid species have been made available in recent years, such as for Rainbow trout (Oncorhynchus mykiss, Berthelot et al 2014;Pearse et al 2018), Atlantic salmon (Salmo salar, Lien et al 2016), Grayling (Thymallus thymallus, Varadharajan et al 2018;Sävilammi et al 2019), Chinhook salmon (Oncorhynchus tshawytscha, Christensen, Leong, Sakhrani, Biagi, Minkley, Withler, Rondeau, Koop and Devlin 2018) and one more (Coho salmon, Oncorhynchus kisutch) is available on NCBI (Genebank assembly GCA_002021735.1). About 88-103 million years ago an ancestor of Salmonids underwent a whole genome duplication (Ss4R), the fourth on the vertebrate lineage (Allendorf and Thorgaard 1984;Macqueen and Johnston 2014;Berthelot et al 2014).…”

Simulation with RADinitio Improves RADseq Experimental Design and Sheds Light on Sources of Missing Data

“…Under this metric, the char's locus distribution appears more similar to the grayling's despite greater evolutionary distance. They do, however, share similar rediploidization histories following the salmonid genome duplication (Christensen et al, 2018;Varadharajan et al, 2018) and comparable genome architecture. The northern pike, a species sister to salmonids, has a smaller number of loci, which is expected given its smaller genome, and would thus not serve as an adequate model for estimating RAD loci in the brown trout unless there were no alternatives.…”