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Extensive Hybridization Following a Large Escape of Domesticated Atlantic Salmon in the Northwest Atlantic

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Extensive Hybridization Following a Large Escape of Domesticated Atlantic Salmon in the Northwest Atlantic

Brendan F Wringe et al. Commun Biol.

Abstract

Domestication is rife with episodes of interbreeding between cultured and wild populations, potentially challenging adaptive variation in the wild. In Atlantic salmon, Salmo salar, the number of domesticated individuals far exceeds wild individuals, and escape events occur regularly, yet evidence of the magnitude and geographic scale of interbreeding resulting from individual escape events is lacking. We screened juvenile Atlantic salmon using 95 single nucleotide polymorphisms following a single, large aquaculture escape in the Northwest Atlantic and report the landscape-scale detection of hybrid and feral salmon (27.1%, 17/18 rivers). Hybrids were reproductively viable, and observed at higher frequency in smaller wild populations. Repeated annual sampling of this cohort revealed decreases in the presence of hybrid and feral offspring over time. These results link previous observations of escaped salmon in rivers with reports of population genetic change, and demonstrate the potential negative consequences of escapes from net-pen aquaculture on wild populations.

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Geographic distribution of sampling relative to aquaculture escape event and genome-wide comparison of wild and domestic salmon. a Map of southern Newfoundland, location relative to eastern Canada shown in inset. Black dots represent rivers surveyed; the red dot denotes the location of the 2013 aquaculture escape event. b Manhattan plot illustrating the genome-wide genetic differentiation (FST) between the wild and aquaculture baseline samples (Supplementary Table 7) used in the validation of the SNP panel accuracy. The red circles indicate the loci included in the 95 SNP collectively diagnostic panel. Linkage positions are from Brenna-Hansen et al.
Fig. 2
Fig. 2
Accuracy of detection of each of the genotype frequency classes across a range of critical posterior probability thresholds for the 95 SNP panel used in this study. The black line represents the mean of three replicate analyses of each of three independently simulated datasets and the dotted lines are the standard deviation. The vertical blue line is meant to highlight the critical posterior probability of assignment threshold (>0.8) used in this study
Fig. 3
Fig. 3
Distribution and extent of hybridization following a large escape event of domestic Atlantic salmon. a Geographic distribution of wild, feral, or hybrid young-of-the-year Atlantic salmon across sample locations in 2014. b River-specific proportions of hybrid young-of-the-year salmon partitioned by hybrid genotype class (i.e., F1, F2, backcross wild (BCW), and backcross farm (BCF)). The open circle indicates a sample in which no hybrids were found, the asterisk signifies a location where accurate assignment to hybrid class was not possible. Bar graphs represent the overall proportions of each class in the entire sampling range, taking into account the varying sizes of the sampled populations (i.e., weighting by the axial distance, the distance along a straight line along the longest axis of the river), and colors therein are used as the legend
Fig. 4
Fig. 4
Association between wild population size and levels of hybridization. a River axial distance (i.e., the distance along a straight line along the longest axis of the river). b Relationship between river axial distance and the proportions of wild, feral, and all hybrid (i.e., sum of proportions of F1, F2, BC wild, and BC farm) young-of-the-year Atlantic salmon sampled in 2014. c Relationship between mean number of salmon angled (2010–2014) and the proportions of wild, feral, and hybrid young-of-the-year Atlantic salmon sampled in 2014. The gray shading is the 95% CI of the prediction of the linear models. See Supplementary Table 4 for model parameter estimates
Fig. 5
Fig. 5
Temporal variation (2014–2015) in levels of hybridization. a River specific and overall trends in the proportion of wild, feral, and hybrid young-of-the-year Atlantic salmon between 2014 and 2015. Gray shaded boxplots illustrate the overall proportions across all rivers, midline represents the medians, the upper and lower bounds the interquartile ranges, and the whiskers extend to 1.5 times the interquartile range. Black dots represent the mean difference (±SE) between 2014 and 2015 in the proportion of each pure and hybrid class present. All hybrids is the sum of proportions of F1, F2, BC wild, and BC farm. b River specific and overall trends in the proportion of wild, feral, and hybrid young-of-the-year and one year old (1+) Atlantic salmon sampled in 2014 and 2015, respectively. Gray shaded boxplots illustrate the overall proportions across all rivers. The midline represents the medians, the upper and lower bounds the interquartile ranges, and the whiskers extend to 1.5 times the interquartile range. Black dots represent the mean difference (±SE) across rivers between 2014 and 2015 in the proportion of each pure and hybrid class present of young-of-the-year and 1-year-old individuals. All hybrids is the sum of proportions of F1, F2, BC wild, and BC farm. See Fig. 1 and Table 1 for location information, and sample sizes

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