Plastic and adaptive mitochondrial responses help face hypoxia events in a freshwater fish

Abstract Hypoxic events (i.e. reduction of dissolved oxygen in water) are natural events, which intensity and frequency have been amplified by human activities. As oxygen fuels aerobic metabolism, species unable to avoid those events must maintain their functions through phenotypic adjustments, that could occur both at the individual level (plasticity) and population genomic level (adaptation). To examine the adaptative and plastic responses to hypoxia, we exposed two generations of three‐spined sticklebacks, Gasterosteus aculeatus , from wild populations historically exposed to different oxygen levels, to two different experimental oxygen conditions (normoxia or intermittent hypoxia with 12 h normoxia: 12 h hypoxia; with nighttime O 2 level at 20% for wild‐caught F0 during 4–6 weeks and at 35% for F1 throughout their entire 19‐month lifetime). By comparing the two generations, early‐life programming of the mitochondrial aerobic metabolism was revealed, conditioning the adult‐stage phenotypic and plastic response: F0 fish from the wild hypoxic environment had elevated pectoral muscle mitochondrial respiration and were able to increase their mitochondrial OXPHOS control efficiency under normoxia conditions at the adult stage. Signs of adaptations towards mitochondrial suppression were found in F1 hypoxia population fish livers while no differences were observed in their pectoral muscle, suggesting a downregulation of the hepatic, but not the pectoral muscle, aerobic activities through generations. In opposition to the adaptative trend, the plastic responses to experimental hypoxia were a decreased mitochondrial respiration in the pectoral muscle and an elevated liver mitochondrial oxidative phosphorylation of the F1 fish, suggesting that inherited divergence rather countered than reinforced plastic responses. While both signs of adaptation and plasticity were found in the antioxidant defences of F1 fish, the absence of significant differences between experimental groups in terms of oxidative damage revealed that these fish were able to maintain oxidative balance. Our findings highlight that plasticity to hypoxia depends on the full organism life‐cycle, with the adult ability to face hypoxia depending on their early‐life environmental experience and provides valuable information on the potential evolutionary process of fish facing hypoxia. Read the free Plain Language Summary for this article on the Journal blog.