A European Whitefish Linkage Map and Its Implications for Understanding Genome-Wide Synteny Between Salmonids Following Whole Genome Duplication

Abstract

Genomic datasets continue to increase in number due to the ease of production for a wider selection of species including non-model organisms. For many of these species, especially those with large or polyploid genomes, highly contiguous and well-annotated genomes are still rare due to the complexity and cost involved in their assembly. As a result, a common starting point for genomic work in non-model species is the production of a linkage map. Dense linkage maps facilitate the analysis of genomic data in a variety of ways, from broad scale observations regarding genome structure e.g., chromosome number and type or sex-related structural differences, to fine scale patterns e.g., recombination rate variation and co-localization of differentiated regions. Here we present both sex-averaged and sex-specific linkage maps for Coregonus sp. “Albock”, a member of the European whitefish lineage (C. lavaretus spp. complex), containing 5395 single nucleotide polymorphism (SNP) loci across 40 linkage groups to facilitate future investigation into the genomic basis of whitefish adaptation and speciation. The map was produced using restriction-site associated digestion (RAD) sequencing data from two wild-caught parents and 156 F1 offspring. We discuss the differences between our sex-averaged and sex-specific maps and identify genome-wide synteny between C. sp. “Albock” and Atlantic Salmon (Salmo salar), which have diverged following the salmonid-specific whole genome duplication. Our analysis confirms that many patterns of synteny observed between Atlantic Salmon and Oncorhynchus and Salvelinus species are also shared by members of the Coregoninae subfamily. We also show that regions known for their species-specific rediploidization history can pose challenges for synteny identification since these regions have diverged independently in each salmonid species following the salmonid-specific whole genome duplication. The European whitefish map provided here will enable future studies to understand the distribution of loci of interest, e.g., FST outliers, along the whitefish genome as well as assisting with the de novo assembly of a whitefish reference genome.

Comparative Genomic Analyses and a Novel Linkage Map for Cisco (Coregonus artedi) Provide Insights into Chromosomal Evolution and Rediploidization Across Salmonids

“…The main focus of our comparative analysis was to define the homologous and homeologous relationships among the linkage groups available for the coregonines, specifically in cisco (current study), lake whitefish ( Gagnaire et al 2013 ), and European whitefish ( De-Kayne and Feulner 2018 ), and bring these species into the context of the broader chromosomal correspondence within the lineage by identifying the homologous chromosome arms in brook trout, Atlantic salmon, and Chinook salmon, as well as the non-duplicated northern pike ( Table 2 , Supplementary file S5). To facilitate these comparisons, we applied the same chromosome identification system as used by Sutherland et al (2016) , here termed the “protokaryotype identifier (PK)” system.…”

“…Most PKs were identifiable in the mapcomp analysis conducted here, with some notable exceptions for each coregonine species. In cisco, chromosome arms PK 22.2, 25.1 and 25.2 were unidentified; two of these arms (PK 25.1 and 25.2) were also unidentified in the European whitefish linkage map ( De-Kayne and Feulner 2018 ). Additionally, it was difficult to determine correspondences for PK 09 and 23.…”

“…This degree of uncertainty was much higher than documented in Salmo, Oncorhynchus, and Salvelinus by Sutherland et al (2016), where there were only two ambiguities across these groups. Coregonines appear to have a number of relatively small acrocentric chromosomes (Phillips and Rab 2001), some of which contain a high degree of duplicated loci, making constructing linkage maps more difficult than for other salmonids (Gagnaire et al 2013;De-Kayne and Feulner 2018). For example, PK 25 has never been successfully mapped in coregonines, likely because it is small, submetacentric or acrocentric, and contains many duplicates.…”

“…mapcomp can be used to compare syntenic relationships among markers between linkage maps of any related species using a genome intermediate from another related species ( Sutherland et al 2016 ). Here, mapcomp was used to compare the cisco map with other Coregonus spp., including lake whitefish C. clupeaformis ( Gagnaire et al 2013 ), European whitefish C. lavaretus “Albock” ( De-Kayne and Feulner 2018 ), as well as other representative species from other salmonid genera ( i.e. , Atlantic salmon ( Lien et al 2016 ), brook trout S. fontinalis ( Sutherland et al 2016 ), and Chinook salmon ( Brieuc et al 2014 ) and a representative outgroup to the salmonid WGD, northern pike Esox lucius ( Rondeau et al 2014 )).…”

Mapping of Adaptive Traits Enabled by a High-Density Linkage Map for Lake Trout

“…Linkage maps have been constructed for multiple salmonid species including rainbow trout (Miller et al 2012;Palti et al 2012;Gonzalez-Pena et al 2016), chinook salmon (Brieuc et al 2014;McKinney et al 2016;McKinney et al 2019), coho salmon (Kodama et al 2014), sockeye salmon (Everett, Miller and Seeb 2012;Larson et al 2015;Limborg et al 2015), chum salmon (Waples et al 2016); pink salmon (Spruell et al 1999;Lindner et al 2000), Atlantic salmon (Moen et al 2008;Lien et al 2011;Brenna-Hansen et al 2012;Gonen et al 2014), Arctic char (Nugent et al 2017;Christensen et al 2018a), brook trout (Sauvage et al 2012;Sutherland et al 2016;Hale et al 2017), brown trout (Leitwein et al 2017), European grayling (Sävilammi et al 2019), lake whitefish (Rogers et al 2007;Gagnaire et al 2013a), and European whitefish (De-Kayne et al 2018). No linkage map has been constructed for lake trout (but see May et al 1979, Johnson et al 1987, for work on segregation patterns in lake trout x brook trout hybrids), although the lake trout karyotype has been characterized in multiple previous studies (Phillips and Zajicek 1982;Reed and Phillips 1995) providing a reference for the number of expected chromosomes.…”