Distinct early-life stage gene expression effects of hybridization among European and North American farmed and wild Atlantic salmon populations

Due to multi-generation domestication selection, farmed and wild Atlantic salmon diverge genetically, which raises concerns about potential genetic interactions among escaped farmed and wild populations and disrupts local adaptation through introgression. When farmed strains of distant geographic origin are used, it is unknown whether the genetic risks posed by escaped farmed fish will be greater than if more locally derived strains are used. Quantifying gene expression differences among divergent farmed, wild and F1 hybrids under controlled conditions is one of the ways to explore the consequences of hybridization. We compared the transcriptomes of late sac fry of a European (EO) farmed (“StofnFiskur”, Norwegian strain), a North American (NA) farmed (Saint John River, NB strain), a Newfoundland (NF) wild population with EO ancestry, and related F1 hybrids using 44K microarrays. Our findings indicate that the wild population showed greater transcriptome differences from the EO farmed strain than that of the NA farmed strain. We also found the largest differences in global gene expression between the two farmed strains. We detected fewer differentially expressed transcripts between F1 hybrids and domesticated/wild maternal strains. We also found that the differentially expressed genes between cross types over-represented GO terms associated with metabolism, development, growth, immune response, and redox homeostasis processes. These findings suggest that the interbreeding of escaped EO/NA farmed and NF wild population would alter gene transcription, and the consequences of hybridization would be greater from escaped EO farmed than NA farmed salmon, resulting in potential effects on the fitness of wild populations. Salmon used in experimental crosses were derived from parental salmon of three main populations: Farm.NA, Farm.EO, and Wild. The origin of Farm.NA is the Saint John River, New Brunswick, Canada. Farm.NA gametes were collected from the aquaculture company Northern Harvest, based in Southern Newfoundland, Canada. Farm.EO, a Norwegian origin farm strain, is now produced at an Icelandic facility (StofnFiskur), from where the gametes were shipped by air for the experimental crosses. The wild population was derived from the Northeast Placentia River, Newfoundland, Canada. The microarray study was performed using a consortium for Genomic Research on All Salmonids Project (cGRASP)-designed Agilent (Mississauga, ON, CA) 44K salmonid oligonucleotide microarray (GEO accession number: GPL11299. The microarray experiment comprised 36 arrays: 6 cross types (Farm.NA, Hyb.NAff, Wild, Hyb.EOwf, Hyb.EOff, and Farm.EO) x 3 families per cross type x 2 biological replicates per family. F1 Farm.NA(f)-x-Wild(m) hybrid (referred to as “Hyb.NAff”); F1 Farm.EO(m)-x-Wild(f) hybrid (referred to as “HybEOwf”); and F1 Farm.EO(f)-x-Wild(m) hybrid (referred to as “Hyb.EOff”). variable: Farm.NA: Farm.NA1, Farm.NA2, Farm.NA3, Farm.NA4, Farm.NA5, Farm.NA6 variable: Hyb.NAff: Hyb.NAff1, Hyb.NAff2, Hyb.NAff3, Hyb.NAff4, Hyb.NAff5, Hyb.NAff6 variable: Wild: Wild1, Wild2, Wild3, Wild4, Wild5, Wild6 variable: Hyb.EOwf: Hyb.EOwf1, Hyb.EOwf2, Hyb.EOwf3, Hyb.EOwf4, Hyb.EOwf5, Hyb.EOwf6 variable: Hyb.EOff: Hyb.EOff1, Hyb.EOff2, Hyb.EOff3, Hyb.EOff4, Hyb.EOff5, Hyb.EOff6 variable: Farm.EO: Farm.EO1, Farm.EO2, Farm.EO3, Farm.EO4, Farm.EO5, Farm.EO6