Background.
Atlantic salmon (Salmo salar) is one of the most economically important aquaculture species and a major contributor to the global supply of high-quality protein. As salmon breeding programmes have advanced from pedigree-based selection to the use of genome-wide marker data, managing genetic diversity has become increasingly important for sustaining long-term genetic gain and breeding programme sustainability (��deg��rd et al., 2014; Tsai et al., 2017). Reconstructing demographic history in salmon is challenging, since estimates of effective population size (Ne) can be skewed due to the anadromous life cycle, population structure, varying recombination rates, and the whole genome duplication event that salmon genomes underwent in the distant past (Palstra et al., 2009; Rougemont et al., 2023). Estimating historical Ne more accurately can help better understand current patterns of diversity as observed in farmed and wild populations. Estimating Ne is crucial for preserving genetic diversity and can inform selective breeding programmes to improve their efficiency (Houston et al., 2020).
Aims
The aims of this study were to reconstruct the demographic history of Atlantic salmon across recent and ancient timescales using linkage disequilibrium (GONE software) and Pairwise Sequentially Markovian Coalescent (PSMC) methodologies. Further, sensitivity analyses were conducted to test how genomic regions retaining duplicated loci after the rediploidisation process (residual tetraploidy) and regional differences in recombination might affect Ne estimates.
Materials and Methods
Whole-genome sequence data from 74 Atlantic salmon were analysed to study their demographic history in recent and distant evolutionary periods. The dataset used included wild populations from Canada (30 samples) and Norway (26), together with a farmed population from Scotland (18). To assess genetic variation and population structure among populations, principal component analysis (PCA) and pairwise FST were estimated in PLINK v1.90b7.2, while ancestry proportions were inferred using ADMIXTURE v1.3.0 (Liu et al., 2020). Recent Ne changes (1 to 1,000 years) were estimated using GONE (Santiago et al., 2020). For ancient demographic history (1,000 to 1,000,000 years ago), the PSMC method was used (Li & Durbin, 2011). Sensitivity analyses were performed by excluding genome regions showing evidence of residual tetrasomy, including pericentromeric regions, and by restricting analysis to uniquely mapped regions.
Results
PCA showed that the Canadian Atlantic salmon samples were more distinct compared to the European Atlantic salmon, with Scottish and Norwegian salmon being more similar to each other. The ADMIXTURE analysis confirmed a mixed ancestry between Scottish and Norwegian populations. For ancient history, PSMC showed similar demographic trends across populations, with Ne declining from approximately 100,000 one million years ago to approximately 5,000 by 7,000 years ago, followed by varying peaks across populations towards the recent end of the trajectory. In contrast for recent history, GONE showed different regional magnitudes; Norway and Scotland had higher Ne than the Canadian samples, before they declined sharply towards the present to values close to 100, whereas the Canadian population retained higher Ne of ~ 1000. Sensitivity analyses did not substantially alter these historical Ne patterns, indicating that estimates are robust.
Discussions and Conclusions
This analysis provides a framework to combine recent and more ancient history estimation methodologies to obtain robust historical trajectories of Ne. Our results showed a clear regional differentiation between North American and European Atlantic salmon, as expected, and less differentiation between farmed Scottish and wild Norwegian populations. This can be explained by the development of modern breeding programmes in Europe, where founder populations often had a common origin. This is likely to have resulted in lower genetic divergence between them. Although it was shown that all populations shared broadly similar ancient Ne patterns, more recent demographic inference varies by geographical region. The observed demographic patterns remained stable even when accounting for residual tetraploidy and varying recombination rates. These findings provide a robust overview of Atlantic salmon recent and ancient demographic history. This work contributes useful insights into the processes shaping Atlantic salmon diversity and effective population size, offering essential context for breeding programme strategies and the management of diversity in farmed populations..
References
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