Chromosomal differences between European and North American Atlantic salmon discovered by linkage mapping and supported by fluorescence in situ hybridization analysis

Abstract

Background: Geographical isolation has generated a distinct difference between Atlantic salmon of European and North American Atlantic origin. The European Atlantic salmon generally has 29 pairs of chromosomes and 74 chromosome arms whereas it has been reported that the North American Atlantic salmon has 27 chromosome pairs and an NF of 72. In order to predict the major chromosomal rearrangements causing these differences, we constructed a dense linkage map for Atlantic salmon of North American origin and compared it with the well-developed map for European Atlantic salmon.

Results: The presented male and female genetic maps for the North American subspecies of Atlantic salmon, contains 3,662 SNPs located on 27 linkage groups. The total lengths of the female and male linkage maps were 2,153 cM and 968 cM respectively, with males characteristically showing recombination only at the telomeres. We compared these maps with recently published SNP maps from European Atlantic salmon, and predicted three chromosomal reorganization events that we then tested using fluorescence in situ hybridization (FISH) analysis. The proposed rearrangements, which define the differences in the karyotypes of the North American Atlantic salmon relative to the European Atlantic salmon, include the translocation of the p arm of ssa01 to ssa23 and polymorphic fusions: ssa26 with ssa28, and ssa08 with ssa29.

Conclusions: This study identified major chromosomal differences between European and North American Atlantic salmon. However, while gross structural differences were significant, the order of genetic markers at the fine-resolution scale was remarkably conserved. This is a good indication that information from the International Cooperation to Sequence the Atlantic salmon Genome, which is sequencing a European Atlantic salmon, can be transferred to Atlantic salmon from North America.

Figure 1

A translocation involving the European ssa01 p-arm and ssa23 to create a metacentric chromosome in North American salmon (ssa01p/23). The European ssa01 (red) and ssa23 (green) are shown to the right and the new acrocentric chromosome in North American salmon to the left. Numbers correspond to SNPs listed in Additional file 1. SNPs in colors are shared between Atlantic salmon from both sides of the Atlantic Ocean. Red lines extend to the set of SNPs with limited recombination in the male map.

Figure 2

A chromosomal fission of European ssa01 creating an acrocentric chromosome in North American Atlantic salmon (ssa01q-fission). The European ssa01 is shown to the right and the new acrocentric chromosome in North American salmon is shown to the left. Numbers correspond to SNPs listed in Additional file 1. SNPs in colors are shared between Atlantic salmon from both sides of the Atlantic Ocean. Red lines extend to the set of SNPs with limited recombination in the male map.

Figure 3

Genetic map of North American Atlantic salmon chromosome ssa26/28. The proposed chromosome is to the left and the corresponding European Atlantic salmon chromosome(s) to the right. Numbers correspond to SNPs listed in Additional file 1. SNPs in colors are shared between Atlantic salmon from both sides of the Atlantic Ocean. Red lines extend to the set of SNPs with limited recombination in the male map. The chromosome consists of the two small acrocentric European chromosomes ssa26 (red) and ssa28 (green) fused head to head. The new chromosome ssa26/28 is metacentric.

Figure 4

Genetic map of North American Atlantic salmon chromosome ssa08/29. The proposed chromosome is to the left and the corresponding European Atlantic salmon chromosome(s) to the right. Numbers correspond to SNPs listed in Additional file 1. SNPs in colors are shared between Atlantic salmon from both sides of the Atlantic Ocean. Red lines extend to the set of SNPs with limited recombination in the male map. The chromosome consists of the metacentric European ssa08 (red) fused with the acrocentric European ssa29 (green) tail to head, causing a predicted centromere shift to the fusion point. The new chromosome ssa8/29 is metacentric.

Figure 5

Ssa01p/23 FISH-images with arrows pointing at BAC probes. Metaphase spreads of a North American Atlantic salmon from Aqua Bounty Canada and a European Atlantic salmon. Red label with red arrow: BAC S0198E23 on ssa01p. Red label with yellow arrow: BAC S0088O23 on ssa01q. Green label: BAC S0102N22 on ssa23. 1: European Atlantic salmon: The red signals go to a large metacentric chromosome in the European sample, and the green signal is visible on a small acrocentric. 2: North American Atlantic salmon: In the North American salmon the red signals are separated. Instead of the large metacentric we see two large acrocentric chromosomes with one red signal, and two smaller metacentric chromosomes with red and green signals.

Figure 6

Ssa26/28 FISH-images with arrows pointing at BAC probes. Metaphase spreads of a male North American Atlantic salmon from Aqua Bounty Canada and a European Atlantic salmon. Red label: BAC S0059P02 on ssa26, Green label: BAC S0091M08 on ssa28. 1: European Atlantic salmon: The signals were found on different acrocentric chromosome pairs in the European sample. 2: North American Atlantic salmon: The signals were joined on a metacentric chromosome in the North American salmon (fusion of ssa26 and ssa 28) and on the two unfused acrocentric chromosomes (ssa26 and ssa28), indicating that this North American Atlantic salmon is heterozygous for the fusion.

Figure 7

FISH-images of ssa08/29 with arrows pointing at BAC probes. Metaphase spreads of a North American Atlantic salmon from Aqua Bounty Canada and a European Atlantic salmon. Red label: BAC S0214J02 on ssa8, Green label: BAC S0016D16 on ssa29 1: European Atlantic salmon: As predicted the signals go to individual chromosomes in the European sample. Note the intense light blue stain of heterochromatin on ssa08, which is where the rRNA genes are located. 2: North American Atlantic salmon: The signals co-locate to separate chromosomes (fusion of ssa08 and ssa29) and also to the two unfused acrocentric chromosomes (ssa08 and ssa29), indicating that this North American Atlantic salmon is heterozygous for the fusion.