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

BACKGROUND: Evolutionary processes leave footprints along the genome over time. Highly homozygous regions may correspond to positive selection of favorable alleles, while maintenance of heterozygous regions may be due to balancing selection phenomena. We analyzed data from 176 fish from four disconnected domestic rainbow trout populations that were genotyped using a high-density Axiom Trout genotyping 665K single nucleotide polymorphism array, including 20 from the US and 156 from three French lines. Using methods based on runs of homozygosity and extended haplotype homozygosity, we detected signatures of selection in these four populations. RESULTS: Nine genomic regions that included 253 genes were identified as being under positive selection in all four populations Most were located on chromosome 2 but also on chromosomes 12, 15, 16, and 20. In addition, four heterozygous regions that contain 29 genes that are putatively under balancing selection were also shared by the four populations. These were located on chromosomes 10, 13, and 19. Regardless of the homozygous or heterozygous nature of the regions, in each region, we detected several genes that are highly conserved among vertebrates due to their critical roles in cellular and nuclear organization, embryonic development, or immunity. We identified new candidate genes involved in rainbow trout fitness, as well as 17 genes that were previously identified to be under positive selection, 10 of which in other fishes (auts2, atp1b3, zp4, znf135, igf-1α, brd2, col9a2, mrap2, pbx1, and emilin-3). CONCLUSIONS: Using material from disconnected populations of different origins allowed us to draw a genome-wide map of signatures of positive selection that are shared between these rainbow trout populations, and to identify several regions that are putatively under balancing selection. These results provide a valuable resource for future investigations of the dynamics of genetic diversity and genome evolution during domestication.

Development of a High-Density 665 K SNP Array for Rainbow Trout Genome-Wide Genotyping.

Single nucleotide polymorphism (SNP) arrays, also named « SNP chips ¼, enable very large numbers of individuals to be genotyped at a targeted set of thousands of genome-wide identified markers. We used preexisting variant datasets from USDA, a French commercial line and 30X-coverage whole genome sequencing of INRAE isogenic lines to develop an Affymetrix 665 K SNP array (HD chip) for rainbow trout. In total, we identified 32,372,492 SNPs that were polymorphic in the USDA or INRAE databases. A subset of identified SNPs were selected for inclusion on the chip, prioritizing SNPs whose flanking sequence uniquely aligned to the Swanson reference genome, with homogenous repartition over the genome and the highest Minimum Allele Frequency in both USDA and French databases. Of the 664,531 SNPs which passed the Affymetrix quality filters and were manufactured on the HD chip, 65.3% and 60.9% passed filtering metrics and were polymorphic in two other distinct French commercial populations in which, respectively, 288 and 175 sampled fish were genotyped. Only 576,118 SNPs mapped uniquely on both Swanson and Arlee reference genomes, and 12,071 SNPs did not map at all on the Arlee reference genome. Among those 576,118 SNPs, 38,948 SNPs were kept from the commercially available medium-density 57 K SNP chip. We demonstrate the utility of the HD chip by describing the high rates of linkage disequilibrium at 2-10 kb in the rainbow trout genome in comparison to the linkage disequilibrium observed at 50-100 kb which are usual distances between markers of the medium-density chip.

Temporal and region-specific variations in genome-wide inbreeding effects on female size and reproduction traits of rainbow trout.

Recent studies have shown that current levels of inbreeding, estimated by runs of homozygosity (ROH), are moderate to high in farmed rainbow trout lines. Based on ROH metrics, the aims of our study were to (i) quantify inbreeding effects on female size (postspawning body weight, fork length) and reproduction traits (spawning date, coelomic fluid weight, spawn weight, egg number, average egg weight) in rainbow trout, and (ii) identify both the genomic regions and inbreeding events affecting performance. We analysed the performance of 1346 females under linear animal models including random additive and dominance genetics effects, with fixed covariates accounting for inbreeding effects at different temporal and genomic scales. A significant effect of genome-wide inbreeding (F) was only observed for spawning date and egg weight, with performance variations of +12.3% and -3.8%, respectively, for 0.1 unit increase in F level. At different local genomic scales, we observed highly variable inbreeding effects on the seven traits under study, ranging from increasing to decreasing trait values. As widely reported in the literature, the main scenario observed during this study was a negative impact of recent inbreeding. However, other scenarios such as positive effects of recent inbreeding or negative impacts of old inbreeding were also observed. Although partial dominance appeared to be the main hypothesis explaining inbreeding depression for all the traits studied, the overdominance hypothesis might also play a significant role in inbreeding depression affecting fecundity (egg number and mass) traits in rainbow trout. These findings suggest that region-specific inbreeding can strongly impact performance without necessarily observing genome-wide inbreeding effects. They shed light on the genetic architecture of inbreeding depression and its evolution along the genome over time. The use of region-specific metrics may enable breeders to more accurately manage the trade-off between genetic merit and the undesirable side effects associated with inbreeding.