A SNP Based Linkage Map of the Arctic Charr (Salvelinus alpinus) Genome Provides Insights into the Diploidization Process After Whole Genome Duplication

Abstract

Diploidization, which follows whole genome duplication events, does not occur evenly across the genome. In salmonid fishes, certain pairs of homeologous chromosomes preserve tetraploid loci in higher frequencies toward the telomeres due to residual tetrasomic inheritance. Research suggests this occurs only in homeologous pairs where one chromosome arm has undergone a fusion event. We present a linkage map for Arctic charr (Salvelinus alpinus), a salmonid species with relatively fewer chromosome fusions. Genotype by sequencing identified 19,418 SNPs, and a linkage map consisting of 4508 markers was constructed from a subset of high quality SNPs and microsatellite markers that were used to anchor the new map to previous versions. Both male- and female-specific linkage maps contained the expected number of 39 linkage groups. The chromosome type associated with each linkage group was determined, and 10 stable metacentric chromosomes were identified, along with a chromosome polymorphism involving the sex chromosome AC04. Two instances of a weak form of pseudolinkage were detected in the telomeric regions of homeologous chromosome arms in both female and male linkage maps. Chromosome arm homologies within the Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) genomes were determined. Paralogous sequence variants (PSVs) were identified, and their comparative BLASTn hit locations showed that duplicate markers exist in higher numbers on seven pairs of homeologous arms, previously identified as preserving tetrasomy in salmonid species. Homeologous arm pairs where neither arm has been part of a fusion event in Arctic charr had fewer PSVs, suggesting faster diploidization rates in these regions.

Extensive genetic differentiation between recently evolved sympatric Arctic charr morphs

“…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). Comparisons of several salmonids found significant synteny in their linkage groups (Danzmann et al 2005;Sutherland et al 2016), despite rearrangements (Timusk et al 2011;Nugent et al 2017). Thus a substantial fraction of genes in salmonids are paralogs in large syntenic regions (Nugent et al 2017;Christensen, Rondeau, Minkley, Leong, Nugent, Danzmann, Ferguson, Stadnik, Devlin, Muzzerall, Edwards, Davidson and Koop 2018).…”

“…Comparisons of several salmonids found significant synteny in their linkage groups (Danzmann et al 2005;Sutherland et al 2016), despite rearrangements (Timusk et al 2011;Nugent et al 2017). Thus a substantial fraction of genes in salmonids are paralogs in large syntenic regions (Nugent et al 2017;Christensen, Rondeau, Minkley, Leong, Nugent, Danzmann, Ferguson, Stadnik, Devlin, Muzzerall, Edwards, Davidson and Koop 2018).…”

“…Population genomic data and analyses are needed to disentangle the role of positive selection and intrinsic factors on patterns of differentiation in this system. More broadly, the confirmed synteny of large genomic regions (Nugent et al 2017), the range of species, subspecies and ecologically distinct populations (Klemetsen 2013;Jacobs et al 2018) sets the stage for future studies of the genomic and ecological correlates of divergence and polymorphism in salmonids.…”

Genomics and telemetry suggest a role for migration harshness in determining overwintering habitat choice, but not gene flow, in anadromous Arctic Char

“…An Arctic Char reference genome is in preparation (Macqueen, Primmer, & Houston, 2017), but it was not available at the time these analyses were conducted. Given the absence of a reference genome, we identified approximate locations for the markers using the recently developed high-density linkage map for Arctic Char (Nugent, Easton, Norman, Ferguson, & Danzmann, 2017). To increase the number of markers being positioned, the sex-averaged consensus map was used, including female-and male-specific markers.…”

Sex matters in massive parallel sequencing: Evidence for biases in genetic parameter estimation and investigation of sex determination systems

“…These are chromosome arms 1.2, 14.1, 15.1 and 19.1 as per the Northern Pike chromosome (Esox lucius, Rondeau et al, 2014) naming conventions outlined bySutherland et al (2016). Although previously only a low-density map was available for Arctic Char(Timusk et al, 2011), recently a high-density genetic map was generated and homology comparisons were made with several species, including Chinook Salmon(Nugent, Easton, Norman, Ferguson, & Danzmann, 2017). As the Brook Char map was also corresponded to Chinook Salmon, it was possible to identify which Arctic Char chromosomes contain sex-linked markers from the present study.…”