Genetic architecture of acute hyperthermia resistance in juvenile rainbow trout (Oncorhynchus mykiss) and genetic correlations with production traits

Abstract

Background Selective breeding is a promising solution to reduce the vulnerability of fish farms to heat waves, which are predicted to increase in intensity and frequency. However, limited information about the genetic architecture of acute hyperthermia resistance in fish is available. Two batches of sibs from a rainbow trout commercial line were produced: the first (N = 1382) was phenotyped for acute hyperthermia resistance at nine months of age and the second (N = 1506) was phenotyped for main production traits (growth, body length, muscle fat content and carcass yield) at 20 months of age. Fish were genotyped on a 57 K single nucleotide polymorphism (SNP) array and their genotypes were imputed to high-density based on the parent’s genotypes from a 665 K SNP array. Results The heritability estimate of resistance to acute hyperthermia was 0.29 ± 0.05, confirming the potential of selective breeding for this trait. Since genetic correlations of acute hyperthermia resistance with the main production traits near harvest age were all close to zero, selecting for acute hyperthermia resistance should not impact the main production traits, and vice-versa. A genome-wide association study revealed that resistance to acute hyperthermia is a highly polygenic trait, with six quantitative trait loci (QTL) detected, but explaining less than 5% of the genetic variance. Two of these QTL, including the most significant one, may explain differences in acute hyperthermia resistance across INRAE isogenic lines of rainbow trout. Differences in mean acute hyperthermia resistance phenotypes between homozygotes at the most significant SNP was 69% of the phenotypic standard deviation, showing promising potential for marker-assisted selection. We identified 89 candidate genes within the QTL regions, among which the most convincing functional candidates are dnajc7, hsp70b, nkiras2, cdk12, phb, fkbp10, ddx5, cygb1, enpp7, pdhx and acly. Conclusions This study provides valuable insight into the genetic architecture of acute hyperthermia resistance in juvenile rainbow trout. We show that the selection potential for this trait is substantial and selection for this trait should not be too detrimental to improvement of other traits of interest. Identified functional candidate genes provide new knowledge on the physiological mechanisms involved in acute hyperthermia resistance, such as protein chaperoning, oxidative stress response, homeostasis maintenance and cell survival.

Genomic characterization of dryland adaptation in endangered Anxi cattle in China

“…ENOPH1 is a recently discovered enzyme in the methionine salvage pathway (Wang et al, 2005) that plays a critical role in modulating stress responses and contributing to cellular metabolic processes (Barth et al, 2014;Zhuang et al, 2019). The PDHX gene is a component of the pyruvate dehydrogenase complex and participates in both ATP synthesis and catabolic processes (Lagarde et al, 2023;Li et al, 2021). The SLC16A7 gene encodes a proton-monocarboxylate cotransporter that plays a role in transporting short-chain fatty acids, ketone bodies, and lactic acid (Zhao et al, 2001).…”

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

“…Maintaining genetic diversity in regions related to the immune system may be essential for resilience against various pathogens. In addition, this region on Omy13 has recently been identified as a significant quantitative trait locus (QTL) for resistance to high temperature [ 77 ].…”

Links between behaviour and acute hyperthermia and hypoxia resistance in rainbow trout using isogenic lines

“…The resistance time or the temperature/O2 saturation at loss of equilibrium are considered as the resistance phenotypes (Beitinger et al 2000;Roze et al 2013). Previously, genetic determinism for acute hyperthermia and hypoxia resistances have been demonstrated in rainbow trout (Perry et al 2005;Lagarde et al 2023a;Prchal et al 2023). Especially, Lagarde et al (2023b) showed that some genotypes were more resistant to acute hyperthermia or hypoxia using rainbow trout isogenic lines but without exploring the physiological mechanisms underlying this observed genetic variability.…”

“…Previously, genetic determinism for acute hyperthermia and hypoxia resistance have been demonstrated in rainbow trout (Perry et al, 2005; Lagarde et al, 2023a,b; Prchal et al, 2023). In particular, Lagarde et al (2023b) showed that some genotypes were more resistant to acute hyperthermia or hypoxia using rainbow trout isogenic lines.…”

“…Resistance to acute hyperthermia and hypoxia are phenotypes of interest in fish for numerous fields of research, such as evolutionary biology (Mandic, Todgham & Richards, 2009;Comte & Olden, 2017), stress-coping physiology (Rytkönen et al, 2007;Saravia et al, 2021), forecasts for climate change effects (Messmer et al, 2017;Potts, Mandrak & Chapman, 2021), and genetics for breeding robust animals (Baer & Travis, 2000;Perry et al, 2005;Debes et al, 2021;Lagarde et al, 2023a;Prchal et al, 2023). The methods in use for measuring these resistance phenotypes consist of increasing the temperature of the water for hyperthermia phenotyping or decreasing the O2 saturation of the water for hypoxia phenotyping until the fish lose equilibrium.…”