A dense SNP-based linkage map for Atlantic salmon (Salmo salar) reveals extended chromosome homeologies and striking differences in sex-specific recombination patterns

Abstract

Background: The Atlantic salmon genome is in the process of returning to a diploid state after undergoing a whole genome duplication (WGD) event between 25 and100 million years ago. Existing data on the proportion of paralogous sequence variants (PSVs), multisite variants (MSVs) and other types of complex sequence variation suggest that the rediplodization phase is far from over. The aims of this study were to construct a high density linkage map for Atlantic salmon, to characterize the extent of rediploidization and to improve our understanding of genetic differences between sexes in this species.

Results: A linkage map for Atlantic salmon comprising 29 chromosomes and 5650 single nucleotide polymorphisms (SNPs) was constructed using genotyping data from 3297 fish belonging to 143 families. Of these, 2696 SNPs were generated from ESTs or other gene associated sequences. Homeologous chromosomal regions were identified through the mapping of duplicated SNPs and through the investigation of syntenic relationships between Atlantic salmon and the reference genome sequence of the threespine stickleback (Gasterosteus aculeatus). The sex-specific linkage maps spanned a total of 2402.3 cM in females and 1746.2 cM in males, highlighting a difference in sex specific recombination rate (1.38:1) which is much lower than previously reported in Atlantic salmon. The sexes, however, displayed striking differences in the distribution of recombination sites within linkage groups, with males showing recombination strongly localized to telomeres.

Conclusion: The map presented here represents a valuable resource for addressing important questions of interest to evolution (the process of re-diploidization), aquaculture and salmonid life history biology and not least as a resource to aid the assembly of the forthcoming Atlantic salmon reference genome sequence.

Figure 1

Sex specific linkage maps for Atlantic salmon chromosome 1 (ssa01). The physical size and appearance of the chromosome is adopted from Phillips et al. (2009). Approximate genetic distances are given to the right of the female map and to the left of the male map. The numbers opposite denote indexes to individual markers as given in Additional Data. Markers homologous to chromosome arm segments in stickleback or salmon are indicated with colours correponding with one of the chromosome arms. The approximate separation of the female genetic map is based on this information. Red lines extend to the set of markers with limited recombination in the male map. Large regional differences are seen between the maps, with most of the male recombination taking place near the telomeric ends.

Figure 2

The proportion of MSVs as a percentage of the total number of markers for each Atlantic salmon chromosome.

Figure 3

Figure reporting BLAST matches between markers on homeologous Atlantic salmon chromosomes and stickleback chromosomes. Patterns exist where groups of mapped SNPs from different Salmon chromosomes match a particular chromosome or region in stickleback. Within each grid square the relative hit positions are indicated horizontally for stickleback and vertically for salmon chromosomes. For example, SNPs on Ssa13qa and 15qb (red squares) align to positions across the full length of stickleback chromosome 12, providing evidence that Ssa13qa and 15qb are homeologues.