Abstract

Global losses of biodiversity are occurring at an unprecedented rate, but causes are often unidentified. Genomic data provide an opportunity to isolate drivers of change and even predict future vulnerabilities. Atlantic salmon (Salmo salar) populations have declined range-wide, but factors responsible are poorly understood. Here, we reconstruct changes in effective population size (Ne) in recent decades for 172 range-wide populations using a linkage-based method. Across the North Atlantic, Ne has significantly declined in >60% of populations and declines are consistently temperature-associated. We identify significant polygenic associations with decline, involving genomic regions related to metabolic, developmental, and physiological processes. These regions exhibit changes in presumably adaptive diversity in declining populations consistent with contemporary shifts in body size and phenology. Genomic signatures of widespread population decline and associated risk scores allow direct and potentially predictive links between population fitness and genotype, highlighting the power of genomic resources to assess population vulnerability.

Highlights

  • Global losses of biodiversity are occurring at an unprecedented rate, but causes are often unidentified

  • Two SNPs were identified as decline-associated loci in both continents, and other decline-associated loci found in both continents were located in close proximity to each other

  • Our data suggest high repeatability for scores across >94% of populations when data from the population of interest are excluded in the construction of the risk model. These methods may offer a novel tool for fisheries managers to identify populations most susceptible to future losses. It has been over two decades since scientists first asked why there are not more Atlantic salmon in the wild[12]

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Summary

Introduction

Global losses of biodiversity are occurring at an unprecedented rate, but causes are often unidentified. We identify significant polygenic associations with decline, involving genomic regions related to metabolic, developmental, and physiological processes. These regions exhibit changes in presumably adaptive diversity in declining populations consistent with contemporary shifts in body size and phenology. With advances in analytical methods, temporal changes in contemporary Ne (~20–25 generations) can be reconstructed from one sampling point using genomic data and genetic linkage information[10,11], allowing characterisation of population trends without intensive long-term sampling. We use genomic data to reconstruct trends in population size across the range of Atlantic salmon and identify populations that have experienced significant declines in recent decades, allowing the investigation of environmental, anthropogenic, and genomic correlates of decline. Focusing on recent declines (~6–7 generations), we found that 60% and 61%

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