Genome-wide detection of positive and balancing selection signatures shared by four domesticated rainbow trout populations (Oncorhynchus mykiss)

Evolutionary processes leave footprints across the genome over time. Highly homozygous regions may correspond to positive selection of favourable alleles, while maintenance of heterozygous regions may be due to balancing selection phenomena. We analyzed 176 genomes coming from 20 sequenced US fish and 156 fish from three different French lines that were genotyped using a HD Axiom Trout Genotyping 665K SNP Array. Using methods based on either Run of Homozygosity or Extended Haplotype Homozygosity, we detected selection signals in four domesticated rainbow trout populations. Nine genomic regions composed of 253 genes, mainly located on chromosome 2 but also on chromosomes 12, 15, 16, and 20, were identified under positive selection in all four populations. In addition, four heterozygous regions containing 29 genes putatively under balancing selection were also shared by the four populations and located on chromosomes 10, 13, and 19. Whatever the homozygous or heterozygous nature of the region, we always found some genes highly conserved among vertebrates due to their critical roles in cellular and nuclear organisation, embryonic development or immunity. We identify new promising candidate genes involved in rainbow trout fitness, as well as genes already detected under positive selection in other fishes (auts2, atp1b3, zp4, znf135, igf-1α, brd2, col9a2, mrap2, pbx1, emilin-3). These findings represent a genome-wide map of signatures of selection common over rainbow trout populations, which is the foundation to understand the processes in action and to identify what kind of diversity should be preserved, or conversely avoided in breeding programs, in order to maintain or improve essential biological functions in domesticated rainbow trout populations.