Identification of Multiple QTL Hotspots in Sockeye Salmon (Oncorhynchus nerka) Using Genotyping-by-Sequencing and a Dense Linkage Map

Abstract

Understanding the genetic architecture of phenotypic traits can provide important information about the mechanisms and genomic regions involved in local adaptation and speciation. Here, we used genotyping-by-sequencing and a combination of previously published and newly generated data to construct sex-specific linkage maps for sockeye salmon (Oncorhynchus nerka). We then used the denser female linkage map to conduct quantitative trait locus (QTL) analysis for 4 phenotypic traits in 3 families. The female linkage map consisted of 6322 loci distributed across 29 linkage groups and was 4082 cM long, and the male map contained 2179 loci found on 28 linkage groups and was 2291 cM long. We found 26 QTL: 6 for thermotolerance, 5 for length, 9 for weight, and 6 for condition factor. QTL were distributed nonrandomly across the genome and were often found in hotspots containing multiple QTL for a variety of phenotypic traits. These hotspots may represent adaptively important regions and are excellent candidates for future research. Comparing our results with studies in other salmonids revealed several regions with overlapping QTL for the same phenotypic trait, indicating these regions may be adaptively important across multiple species. Altogether, our study demonstrates the utility of genomic data for investigating the genetic basis of important phenotypic traits. Additionally, the linkage map created here will enable future research on the genetic basis of phenotypic traits in salmon.

Salmonid chromosome evolution as revealed by a novel method for comparing RADseq linkage maps

“…Assignment of linkage groups to chromosome arms has been performed using fluorescence in situ hybridization with BAC probes for Atlantic Salmon (Phillips et al 2009) and Rainbow Trout (Phillips et al 2006), and synteny has been designated using homologous microsatellite and RADseq markers (using the same library preparation protocols) among Chinook Salmon, Coho Salmon, Rainbow Trout and Atlantic Salmon (Danzmann et al 2008; Phillips et al 2009; Naish et al 2013; Brieuc et al 2014; Kodama et al 2014) and recently Sockeye Salmon (Larson et al 2016). A full comparison across all existing maps has yet to be completed.…”

“…Genome Size ( C value) (Gregory 2016)Exp. Genome Size (Gbp)Northern Pike a (Rondeau et al 2014) Esox lucius EST-based microsatellite (524)250.85–1.400.8–1.4Lake Whitefish (Gagnaire et al 2013) Coregonus clupeaformis RADseq with Sbf I (3,438)402.44–3.442.4–3.4Atlantic Salmon (Lien et al 2011) Salmo salar EST-based SNP chip (5,650)292.98–3.272.8–3.2Brook Charr Salvelinus fontinalis RADseq with Pst I and Msp I (3,826)422.86–3.502.8–3.4Rainbow Trout (Palti et al 2015) Oncorhynchus mykiss RADseq with Sbf I (955)291.87–2.921.8–2.9Coho Salmon (Kodama et al 2014) O. kisutch RADseq with Sbf I (5,377)302.60–3.052.5–3.0Chinook Salmon (Brieuc et al 2014) O. tshawytscha RADseq with Sbf I (6,352)342.45–3.302.4–3.2Pink Salmon (Limborg et al 2014) O. gorbuscha RADseq with Sbf I (7,035)262.23–2.572.2–2.5Chum Salmon (Waples et al 2016) O. keta RADseq with Sbf I (6,119)372.49–2.762.4–2.7Sockeye Salmon (Larson et al 2016) O. nerka RADseq with Sbf I (6,262)292.77–3.042.7–3.0…”

“…This issue is compounded further when different protocols or restriction enzymes are used for library generation. Due to this, it has been suggested to use a common enzyme and protocol to ensure compatibility of maps (Larson et al 2016) to provide markers shared between species similar to shared microsatellite markers (Danzmann et al 2005), but this is not always performed. Here we developed a method to use a related species’ reference genome to integrate linkage maps of different species by pairing homologous and proximate (i.e.…”

“…Although much remains to be understood about rediploidization and residual tetraploidy in salmonids, fundamental work on chromosomal evolution has been conducted using cytogenetics and genetic maps (Phillips & Ráb 2001; Naish et al 2013). From linkage map comparisons using homologous markers, it is known that the same eight pairs of corresponding homeologs are residually tetraploid in Chinook Salmon (Brieuc et al 2014), Coho Salmon (Kodama et al 2014) and Sockeye Salmon (Larson et al 2016), as well as some in Atlantic Salmon although some of these have lower support (Lien et al 2011) . The consistency of these residually tetraploid homeologs indicates that prevention of rediploidization in these chromosomes occurred prior to the divergence of these species (Kodama et al 2014).…”

“…High-density linkage maps have been constructed for Lake Whitefish Coregonus clupeaformis (Gagnaire et al 2013), Atlantic Salmon S. salar (Lien et al 2011; Gonen et al 2014) and members of Oncorhynchus including Rainbow Trout O. mykiss (Miller et al 2012; Palti et al 2015), Chinook Salmon O. tshawytscha (Brieuc et al 2014), Coho salmon O. kisutch (Kodama et al 2014), Pink Salmon O. gorbuscha (Limborg et al 2014), Chum Salmon O. keta (Waples et al 2016) and Sockeye Salmon O. nerka (Everett et al 2012; Larson et al 2016). No high-density maps exist for members of Salvelinus , but low-density microsatellite-based maps exist for Arctic Charr S. alpinus and Brook Charr S. fontinalis (Woram et al 2004; Timusk et al 2011), as well as a low-density (∼300 marker) EST-derived SNP map for S. fontinalis (Sauvage et al 2012a).…”