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Early warming stress on rainbow trout juveniles impairs male reproduction but contrastingly elicits intergenerational thermotolerance.

ABSTRACT: The exposure of adult fish to warm or high temperatures is known to impair reproduction, yet the long-term reproductive impacts for treatments at early life are not well clarified. This study aimed to evaluate the effects of warm temperature (WT) during juvenile stage on gonad maturation, gamete quality, and offspring thermotolerance in rainbow trout. While the comparison of basic reproductive parameters in WT females did not reveal any kind of impairment, many WT males showed an atrophied, undeveloped gonad, or a smaller testis with lower milt volume; sperm quality parameters in WT males and deformity rates in the respective progeny were also highly affected. However, despite of such negative effects, many of the remaining progeny presented better rates of survival and growth when exposed to the same conditions as those of parental fish (WT), suggesting that thermal stress in parr stage males elicited intergenerational thermotolerance after a single generation. The present results support that prolonged warming stress during early life stages can adversely affect key reproductive aspects, but contrastingly increase offspring performance at upper thermal ranges. These findings have implications on the capacity of fish to adapt and to cope with global warming.

SUBMITTER: Butzge AJ

PROVIDER: S-EPMC8382822 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundRainbow trout is a significant fish farming species 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.ResultsA pedigreed population of 1343 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.ConclusionsOur 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.

Project description: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.

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Early warming stress on rainbow trout juveniles impairs male reproduction but contrastingly elicits intergenerational thermotolerance.

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