Farmed salmon strains have been selected to improve growth rates as well as other traits of commercial interest but the 2 million farmed salmon escaping annually may enhance the risk of extinction of wild populations through genetic and ecological interactions. Here, we compare the transcription profiles of 3557 genes in the progeny of farmed and wild Atlantic salmon from Norway and Canada grown in controlled conditions, and demonstrate that five to seven generations of artificial selection led to heritable changes in gene transcription profiles, the average magnitude of the differences being 25% and 18% for at least 1.4% and 1.7% of the expressed genes in juvenile salmon from Norway and Canada, respectively. Moreover, genes showing significant transcription profile differences in both farmed strains (16%) all exhibited parallel changes. These findings, along with the identification of several genes whose expression profiles were modified through artificial selection, provide new insights into the molecular basis of parallel evolution, and suggest how gene flow from farmed escapees may affect the genetic integrity of wild populations.

Large annual escapees of farmed Atlantic salmon enhance the risk of extinction of wild populations through genetic and ecological interactions. Recently, we documented evolutionary change in gene transcription between farmed and wild Atlantic salmon after only five generations of artificial selection. While differences for most quantitative traits are expected to gradually dilute through repeated backcrossing to wild populations, the genetic basis of gene transcription has been shown to be largely nonadditive and hybrid crosses may display unexpected inheritance patterns. This makes it difficult to predict to what extent interbreeding between farmed and wild individuals will change the genetic makeup of wild salmon populations. Here, we compare the genome-wide gene transcription profiles of Norwegian wild salmon to that of a second generation hybrid cross [backcross: (Farmed X Wild) X Wild]. Over 6% (298, q-value < 0.01) of the detected genes exhibited highly significantly different transcription levels, and the range and average magnitude of those differences was strikingly higher than previously described between pure farmed and wild strains. Most differences appear to result from nonadditive gene interactions. These results suggest that interbreeding of fugitive farmed salmon and wild individuals could substantially modify the genetic control of gene transcription in natural populations exposed to high migration from fish farms, resulting in potentially detrimental effects on the survival of these populations. This further supports the idea that measures to considerably reduce the number of escaped farmed salmon and their reproduction in the wild are urgently needed.

Evolutionary genomics has benefited from methods that allow identifying evolutionarily important genomic regions on a genomewide scale, including genome scans and QTL mapping. Recently, genomewide scanning by means of microarrays has permitted assessing gene transcription differences among species or populations. However, the identification of differentially transcribed genes does not in itself suffice to measure the role of selection in driving evolutionary changes in gene transcription. Here, we propose and apply a ''transcriptome scan'' approach to investigating the role of selection in shaping differential profiles of gene transcription among populations. We compared the genomewide transcription levels between two Atlantic salmon subpopulations that have been diverging for only six generations. Following assessment of normality and unimodality on a gene-per-gene basis, the additive genetic basis of gene transcription was estimated using the animal model. Gene transcription h 2 estimates were significant for 1044 (16%) of all detected cDNA clones. In an approach analogous to that of genome scans, we used the distribution of the Q ST values estimated from intra-and intersubpopulation additive genetic components of the transcription profiles to identify 16 outlier genes (average Q ST estimate ¼ 0.11) whose transcription levels are likely to have evolved under the influence of directional selection within six generations only. Overall, this study contributes both empirically and methodologically to the quantitative genetic exploration of gene transcription data.

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BackgroundEcological and evolutionary changes in native populations facing invasion by exotic species are increasingly reported. Recently, it has been shown that competition with exotic rainbow trout (Oncorhynchus mykiss) disrupts dominance hierarchies within groups of native Atlantic salmon (Salmo salar). The genetic and molecular actors underlying phenotypic plasticity are poorly understood.MethodologyHere, we aimed at identifying the genetic and molecular actors contributing to this plastic loss of dominance hierarchies as well as at identifying genes implicated in behaviours related to social dominance. By using microarrays, we compared the genome-wide gene transcription profiles in brains of dominant versus subordinate juvenile Atlantic salmon in presence or absence of a competitive rainbow trout.Principal FindingsAdding the trout competitor resulted in dominant and subordinate salmon being more similar, both behaviourally and at the level of brain gene transcription patterns. Genes for which transcription levels differed between dominant and subordinate salmon in the absence of exotic trout were mainly over-expressed in dominant salmon and included genes implicated in protein turnover, neuronal structural change and oxygen transport.Conclusions/SignificanceOur study provides one of the few examples demonstrating a close interplay between behavioural plasticity and gene transcription, therefore contributing to the understanding of the molecular mechanisms underlying these processes in an ecologically relevant context.

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