Screen for Footprints of Selection during Domestication/Captive Breeding of Atlantic Salmon

Abstract

Domesticated animals provide a unique opportunity to identify genomic targets of artificial selection to the captive environment. Here, we screened three independent domesticated/captive Atlantic salmon (Salmo salar) strains and their wild progenitor populations in an effort to detect potential signals of domestication selection by typing of 261 SNPs and 70 microsatellite loci. By combining information from four different neutrality tests, in total ten genomic regions showed signs of directional selection based on multiple sources of evidence. Most of the identified candidate regions were rather small ranging from zero to a few centimorgans (cM) in the female Atlantic salmon linkage map. We also evaluated how adaptation from standing variation affects adjacent SNP and microsatellite variation along the chromosomes and, by using forward simulations with strong selection, we were able to generate genetic differentiation patterns comparable to the observed data. This study highlights the significance of standing genetic variation during the early stages of adaptation and represents a useful step towards identifying functional variants involved in domestication of Atlantic salmon.

Figure 1

Results of two outlier tests in three independent pairs of wild-reared Atlantic salmon populations. Locus names of putative outliers potentially affected by selection (see Section 3) are indicated. (a) FDIST2: empirical distribution of F _ST against heterozygosity. The solid and dotted lines represent the upper 99% confidence interval for SNPs and tandem repeat markers, respectively; (b) Bayescan: The F _ST estimates plotted against Bayes factor. The dashed lines correspond to the Bayes factor 3 (log10(BF) = 0.5).

Figure 2

Distribution of F _ST along the female and male linkage groups (LGs) in three wild-reared Atlantic salmon pairwise comparisons (IRL, SWE, and CAN). F indicates markers that were identified as outliers at the 99% P level using FDIST2 [26]. B indicates markers that were identified as outliers (log10(Bayes factor) > 0.5) using Bayescan [27]. G indicates clustering of adjacent markers with elevated genetic differentiation (F _ST) (permutation-based significance threshold, P < 0.05). Dashed lines correspond to the upper 2.5% of the empirical F _ST distribution and numbers along the x-axis indicate linkage groups as defined in [28].

Figure 3

Distribution of lnRH along the female and male linkage groups (LGs) in three wild-reared Atlantic salmon pairwise comparisons (IRL, SWE, CAN). G indicates clustering of adjacent markers (permutation-based significance threshold, P < 0.05) that show large differences in genetic diversity measured as lnRH [29]. Dashed lines correspond to the 95% confidence limits (±1.96) of standardized lnRH estimates and numbers along the x-axis indicate linkage groups as defined in [28].

Figure 4

Estimated false discovery rate (FDR) for four different neutrality tests: FDIST2, lnRH, clustering of F _ST and lnRH. Green, blue and red lines correspond to q value estimates for three wild-reared Atlantic salmon pairwise comparisons (IRL, SWE and CAN, resp.).

Figure 5

The effect of positive selection on standing variation on F _ST in three linkage groups (IRL: LG21-Chrom. 26; SWE: LG33-Chrom. 28, CAN: LG6-Chrom. 12). Bold line indicates the empirical distribution of F _ST. Box plots showing the median and interquartile range, nonoutlier range, and outliers and extreme cases from 25 simulation replicates are shown with a line within the rectangle, rectangle, whiskers, cross and an asterisk, respectively. Filled grey rectangles correspond to the markers under selection (positive selection on minor allele); the position of each marker is provided on the x-axis.