Low oxygen concentration in the water, known as hypoxia, occurs naturally but is expected to become more frequent and severe due to current global changes and anthropogenic pressures. Organisms can adjust to a change in their environment via plasticity, but the timing of this plasticity has been overlooked, especially in ecophysiology aspects such as cognition. Cognition, referring to the ability of animals to make decisions, is essential for successful foraging, anti-predatory responses, and many other key functions linked directly to survival. Hypoxia, for instance, may modify different aspect of cognition, like the problem-solving and/or learning/memorizing cognition, what is then crucial to study in the current context of global changes. To address this question, we exposed three groups of three-spined stickleback Gasterosteus aculeatus to different hypoxia regimes: a control group that has always been in normoxia (>90% of O2  throughout the day), a group that has always been exposed to fluctuating hypoxia (>90% of O2  during the day and 30% of O2  during the night to mimic more natural conditions), and a group that has been in normoxia until 4 months-old, and then exposed to fluctuating hypoxia. Their problem-solving and learning/memorizing cognition were assessed using a decision-making and a detour test with an increase of complexity, leading to a reward. Assessing the impact of hypoxia at different developmental stages on cognition provides important insights on the capacity of fish to deal with their changing environments, primordial for predicting the global response of an organism to environmental changes.

Does timing matter? The impact of hypoxia at different developmental stages on fish cognition

Low oxygen concentration events, known as hypoxic events, are naturally occurring but anticipated to become more frequent and severe in the future due to current global changes and anthropogenic pressures. While organisms may adjust their physiology and behaviour in response to hypoxia, better understanding of the link between physiology and behaviour is crucial for predicting the global response of an organism to environmental changes. Even if this link starts to be well known, there is a limited understanding of the genetic basis of it, as well as the potential impact of changing environments on it. Hypoxia, for instance, may modify the correlated evolution between physiology and behaviour by altering the genetic correlation among those traits, what could be important to predict. To address these questions, two populations of Gasterosteus aculeatus were collected from streams already exposed to strong hypoxic events or not. The collected individuals were bred, and half of the offspring were reared either in normoxia (>90% of O2 throughout the day) or hypoxia (>90% of O2 during the day and 30% of O2 during the night to mimic more natural conditions). The growth, swimming capacity, and behaviour (risk-taking and sociability) of the offspring were then measured, and the phenotypic and genetic correlations among the traits estimated. Unravelling the phenotypic and genetic correlations under fluctuating hypoxia can contribute to our understanding of the potential link and evolutionary paths of physiology and behavioural traits facing a changing environment, and the importance of considering that such link may be context dependent.

The missing link: Unravelling the phenotypic and genetic correlation of fish physiology and behaviour under fluctuating hypoxia.

While hypoxia (i.e. low dissolved oxygen level in water) events occur naturally, global change and human activities have exacerbated their strength and temporal fluctuations. As populations may not be able to escape the hypoxic conditions, it is crucial to understand how organisms can adjust and adapt to these fluctuating environments across generations. When directly exposed, individuals may be able to adjust their phenotypes through plasticity to maintain their fitness. With continued exposure to hypoxia over generations, adaptive transgenerational plasticity can take place to help the offspring to survive the new conditions. Even longer exposure could also lead to the evolution of the population. However, so far, little is known on how plastic response to hypoxia could actually pave the way for future evolution. Using two populations of three-spined sticklebacks (Gasterosteus aculeatus) collected from streams already experiencing and potentially adapted to strong hypoxic events or not, we exposed the offspring to experimental hypoxia (30% air saturation during the night and 100% during the day) over three generations, resulting in several groups reflecting within-, inter-, and trans-generational plasticity, as well as adaptation. We then measured their growth, metabolism, and behaviour and highlighted that the plastic responses observed were not necessarily in line to the potential adaptation. While the directions of the responses were different, we cannot exclude that the fish plasticity might still be a strategy to cope with the environment until genetic adaptation occur.

Fish cross-generational response to hypoxia: can plasticity pave the way to evolution?

The frequency of hypoxic events (i.e. decrease of dissolved oxygen level in water) is increasing at an unprecedented rate due to anthropogenic pollution and climate change. As species might not be able to adapt fast enough to this rapid change, they would need to rely on faster phenotypic responses such as plasticity. If the stressor becomes persistent, some transgenerational plasticity could occur. Physiologically the low oxygen environment can impact the organism's metabolism, potentially affecting their fitness. Therefore, more studies are needed to decipher fish metabolisms plasticity to hypoxia within and across generations. To investigate this, we did a multigenerational experiment with a wild population of Gasterosteus aculeatus. The first generation (F1) was either exposed to normoxia (100% dissolved oxygen, DO), or daily fluctuating hypoxia (30% DO at night and 100% DO during the day) mimicking the oxygen fluctuation happening in the wild. Their offspring (F2) were reared either matching their parental condition or not, resulting in four different groups reflecting within- or trans-generational plasticity. We assessed their aerobic metabolism (aerobic scope) and oxygen transport capacity (maximal heart rate frequency, blood hematocrit, and hemoglobin content) as well as the anaerobic metabolism (hypoxia tolerance and Pcrit). The results only showed within plasticity to fluctuating hypoxia with an increased hypoxia tolerance of the fish and decreased Pcrit, while the aerobic metabolism and oxygen transport capacity did not change. This study shows that fish might cope with this level of hypoxia through within-generation plasticity while transgenerational plasticity is not yet observed in measured traits.

Amélie Crespel

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