Temporal change in genetic integrity suggests loss of local adaptation in a wild Atlantic salmon (Salmo salar) population following introgression by farmed escapees

Abstract

In some wild Atlantic salmon populations, rapid declines in numbers of wild returning adults has been associated with an increase in the prevalence of farmed salmon. Studies of phenotypic variation have shown that interbreeding between farmed and wild salmon may lead to loss of local adaptation. Yet, few studies have attempted to assess the impact of interbreeding at the genome level, especially among North American populations. Here, we document temporal changes in the genetic makeup of the severely threatened Magaguadavic River salmon population (Bay of Fundy, Canada), a population that might have been impacted by interbreeding with farmed salmon for nearly 20 years. Wild and farmed individuals caught entering the river from 1980 to 2005 were genotyped at 112 single-nucleotide polymorphisms (SNPs), and/or eight microsatellite loci, to scan for potential shifts in adaptive genetic variation. No significant temporal change in microsatellite-based estimates of allele richness or gene diversity was detected in the wild population, despite its precipitous decline in numbers over the last two decades. This might reflect the effect of introgression from farmed salmon, which was corroborated by temporal change in linkage-disequilibrium. Moreover, SNP genome scans identified a temporal decrease in candidate loci potentially under directional selection. Of particular interest was a SNP previously shown to be strongly associated with an important quantitative trait locus for parr mark number, which retained its genetic distinctiveness between farmed and wild fish longer than other outliers. Overall, these results indicate that farmed escapees have introgressed with wild Magaguadavic salmon resulting in significant alteration of the genetic integrity of the native population, including possible loss of adaptation to wild conditions.

Figure 1

Map showing the Magaguadavic River mouth and the fishway located close to the Passamaquoddy Bay where most of New Brunswick commercial salmon sea-cage sites are in the Bay of Fundy. Modified with permission from Carr et al. (1997) and Carr et al. (2004). (NB, New Brunswick; NS, Nova Scotia; PEI, Prince Edward Island; MA, Maine).

Figure 2

Number of SNP-linked loci per individual SNP locus within population for: (a) FARM-1992, (b) WILD-1992, (c) WILD-1996 (d) WILD -1998_99 and (e) WILD-2002+. Loci are not arranged in the same order among populations but by decreasing order according to the x axis. Median number of linked loci per locus per population (M) and multilocus r_d per population are indicated on each panel. Within population M are not different for populations sharing the same capital letter in the bottom-right corner of panels after Wilcoxon tests (see Results section).

Figure 3

Differentiation (F_ST) as a function of heterozygosity as calculated by FDIST2 when comparing FARM-1992 with: (a) WILD-1992, (b) WILD-1996 (c) WILD -1998_99 and (d) WILD-2002+. On each panel, solid line represent upper and lower 95% confidence level and dotted line indicates the average F_ST across loci. Asterisk (^*) on outliers indicate two values represented by the same dot on the graphic (double asterisks (^**) three values). Only SNP markers were used.

Figure 4

Differentiation (F_ST) of Contig14899_0107 across time as estimated by FDIST2 in genome scans (Figure 3). Wild temporal samples were considered as single year sample based on the sample year predominant in the population (WILD-1996=1996, WILD -1998_99=1999 and WILD-2002+=2002). Regression value is indicated in the top-right corner (P=0.062).