Seasonal decline in mitochondrial plasticity in the three-spined stickleback

preprint OA: closed CC-BY-NC-ND-4.0

Abstract

Mitochondrial plasticity enables ectothermic animals to maintain performance under changing thermal conditions, but whether this ability declines through adulthood is unknown. We explored changes in mitochondrial plasticity in the three-spined stickleback ( Gasterosteus aculeatus ), a temperate fish that in many populations has a single breeding season over which it produces multiple clutches and then dies. Wild-caught fish were exposed to one of three thermal regimes: remaining at 12 °C, switching to constant warm (21 °C) or diel cycling (12–21 °C) for three weeks at either the beginning or end of the season. We quantified both phosphorylating and non-ATP-producing (OXPHOS and LEAK) respiration in isolated muscle mitochondria, and oxidative control efficiency (OxCE). Early in the breeding season, young fish responded to elevated temperatures by adjusting both their capacity for ATP production and non-ATP-production respiration, but this mitochondrial plasticity declined over the season. OxCE was unaffected by time of season or temperature treatment. Changing body condition was unrelated to mitochondrial function. Our findings indicate that mitochondrial plasticity declines across adult life, potentially limiting thermal resilience in older individuals, the first time this has been reported in an ectotherm. This highlights the need to account for age-related physiological changes in capacity when predicting species’ responses to environmental change.
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Abstract Mitochondrial plasticity enables ectothermic animals to maintain performance under changing thermal conditions, but whether this ability declines through adulthood is unknown. We explored changes in mitochondrial plasticity in the three-spined stickleback (Gasterosteus aculeatus), a temperate fish that in many populations has a single breeding season over which it produces multiple clutches and then dies. Wild-caught fish were exposed to one of three thermal regimes: remaining at 12 °C, switching to constant warm (21 °C) or diel cycling (12–21 °C) for three weeks at either the beginning or end of the season. We quantified both phosphorylating and non-ATP-producing (OXPHOS and LEAK) respiration in isolated muscle mitochondria, and oxidative control efficiency (OxCE). Early in the breeding season, young fish responded to elevated temperatures by adjusting both their capacity for ATP production and non-ATP-production respiration, but this mitochondrial plasticity declined over the season. OxCE was unaffected by time of season or temperature treatment. Changing body condition was unrelated to mitochondrial function. Our findings indicate that mitochondrial plasticity declines across adult life, potentially limiting thermal resilience in older individuals, the first time this has been reported in an ectotherm. This highlights the need to account for age-related physiological changes in capacity when predicting species’ responses to environmental change. Competing Interest Statement The authors have declared no competing interest.

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License: CC-BY-NC-ND-4.0