Genetic variation of hypoxia tolerance in farmed fish: a systematic review for selective breeding purposes

Background: Accelerating climate change has intensified hypoxic events in aquatic ecosystems. In aquaculture, high stocking densities make farmed fish particularly vulnerable to these episodes, leading to negative economic repercussions. This has driven interest in selective breeding for hypoxia tolerant fish as a potential mitigation strategy. In this context, the present systematic review synthesizes and critically evaluates current knowledge on genetic variation associated with hypoxia tolerance in farmed fish species. A literature search was conducted in Scopus and Web of Science following the Preferred Reporting Items for Systematic reviews and Meta-Analyses 2020 guidelines. Results: In total, 964 articles were identified, of which 41 met the inclusion criteria, encompassing 26 species and three hybrid lines. Among the farmed fish, the blunt snout bream, rainbow trout, common carp, and Nile tilapia were the most extensively studied. The most commonly used metrics to assess hypoxia tolerance included: (1) time or oxygen level at which loss of equilibrium occurs, (2) survival time or status (alive or dead), and (3) critical oxygen partial tension measured via respirometry. Substantial phenotypic variability in hypoxia tolerance across families, strains, gynogenetic lines, growth transgenic lines, hybrid lines, and species was reported in most studies. Although single nucleotide polymorphism associated with hypoxia tolerance were identified in several studies, heritability estimates were reported in only three of these, ranging from 0.28 to 0.65, underscoring the need for further research to strengthen the basis for selective breeding applications. Furthermore, candidate genes identified across studies were involved in a wide range of biological processes underlying hypoxia responses, including hypoxia signaling and its regulation (HIF-related genes and their inhibitors, such as HIF1αn), angiogenesis, energy metabolism, oxidative stress defense, erythropoiesis, ion regulation, DNA repair, and immune and apoptotic processes. Conclusions: As aquatic environments become more hypoxic, the findings of this review underscore the potential of the inherent genetic diversity for hypoxia tolerance present in farmed fish populations. In this context, genomic selection and gene editing emerge as promising tools for developing hypoxia tolerant fish lines. Further research under production conditions is essential before implementation of these approaches in practical in breeding programs, particularly to evaluate the most appropriate trait(s) for measuring hypoxia tolerance, potential correlated responses with other economically important traits, and the overall feasibility at an industry scale.