Genetic architecture and genomic selection of female reproduction traits in rainbow trout

Abstract

Background Rainbow trout is a significant fish farming industry under temperate climates. Female reproduction traits play an important role in the economy of breeding companies with the sale of fertilized eggs. The objectives of this study are threefold: to estimate the genetic parameters of female reproduction traits, to determine the genetic architecture of these traits by the identification of quantitative trait loci (QTL), and to assess the expected efficiency of a pedigree-based selection (BLUP) or genomic selection for these traits. Results A pedigreed population of 1,343 trout were genotyped for 57,000 SNP markers and phenotyped for seven traits at 2 years of age: spawning date, female body weight before and after spawning, the spawn weight and the egg number of the spawn, the egg average weight and average diameter. Genetic parameters were estimated in multi-trait linear animal models. Heritability estimates were moderate, varying from 0.27 to 0.44. The female body weight was not genetically correlated to any of the reproduction traits. Spawn weight showed strong and favourable genetic correlation with the number of eggs in the spawn and individual egg size traits, but the egg number was uncorrelated to the egg size traits. The genome-wide association studies showed that all traits were very polygenic since less than 10% of the genetic variance was explained by the cumulative effects of the QTLs: for any trait, only 2 to 4 QTLs were detected that explained in-between 1 and 3% of the genetic variance. Genomic selection based on a reference population of only one thousand individuals related to candidates would improve the efficiency of BLUP selection from 16 to 37% depending on traits. Conclusions Our genetic parameter estimates made unlikely the hypothesis that selection for growth could induce any indirect improvement for female reproduction traits. It is thus important to consider direct selection for spawn weight for improving egg production traits in rainbow trout breeding programs. Due to the low proportion of genetic variance explained by the few QTLs detected for each reproduction traits, marker assisted selection cannot be effective. However genomic selection would allow significant gains of accuracy compared to pedigree-based selection.

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

“…This negative inbreeding effect is likely to be unfavourable in terms of fitness, because a large number of eggs is expected to produce a large number of juveniles, at least if egg quality is not altered when egg production is high. While a slight negative phenotypic correlation was observed in our study population between average egg weight and egg number, a null genetic correlation had been estimated between them (D'Ambrosio et al, 2020 ), which corroborates earlier results in the rainbow trout (Su et al, 1996 ). Assuming that egg weight is a good predictor of egg quality, we can hypothesize that the fall in EN and EW values observed with increased inbreeding levels would be unfavourable to fitness in rainbow trout populations.…”

“…As for the fecundity traits spawn weight and egg number, we observed quite similar profiles of temporal and local inbreeding effects, consistent with their high genetic correlation (D'Ambrosio et al, 2020 ). Although we did not estimate any significant genome‐wide inbreeding effect for these two traits, numerous chromosomes displayed significant and high inbreeding effects.…”

“…For example, and as shown in Figure 3 , for average egg weight and Omy1 we observed a small but significant favourable effect on region r3 (from 40 to 60 Mb), but a clearly unfavourable inbreeding effect on region r4 (60 to 80 Mb). Regarding the latter case, several QTLs for egg weight have been detected on the same dataset (D'Ambrosio et al, 2020 ) and deleterious haplotypes have been observed in another French line (Fraslin et al, 2020 ) that might explain inbreeding depression.…”

“…Zooming at the intra‐chromosomal scale, we also observed highly variable effects of local inbreeding on trait performance whatever the chromosome (F omy_ r values are presented in Table S3 ). We focused our analysis on two chromosomes (Figure 3 ): Omy1 containing several QTLs on reproduction traits (D'Ambrosio et al, 2020 ) and Omy10 containing an ROH segment (in the 10_r3 region) shared by diverse rainbow trout populations (D'Ambrosio et al, 2019 ). Along Omy1 (Figure 3 a), highly variable local inbreeding effects were observed, in particular for coelomic fluid weight, with positive effects of the first and last 20‐Mb regions of the chromosome.…”

“…There were around 4 (±2) full‐sibs and 45 (±20) half‐sibs per parent in the phenotyped population under study. Details of the population structure can be found in the article by D'Ambrosio et al ( 2020 ).…”