Understanding how animals cope with environmental change is a central goal of eco-physiology. One common strategy, known as acclimation, is the adjustment of an animal's physiological systems to suit the prevailing conditions. The benefits of acclimation are obvious, as this process allows an animal to maintain performance under a range of environmental conditions. The capacity for acclimation is not universal among animals, however, suggesting that this process may be costly and not always advantageous. However, these theoretical costs have been hard to identify in practice.
To understand these costs, Isabella Loughland and Frank Seebacher, at the University of Sydney, Australia, turned to the mosquitofish Gambusia holbrooki. These tiny tropical fish live in habitats that can change dramatically in temperature, sometimes subjecting the fish to stressfully cold conditions. First, the authors simply asked how well mosquitofish could acclimate to a 10°C temperature change. They raised more than 400 fish under either warm or cold conditions, then put each one in a swim flume (a ‘fish treadmill’) and measured how fast they could swim. Each fish was then exposed to the opposite (warm or cold) temperature, allowed to acclimate for a few weeks, and then their swimming performance was retested at the new temperature.
The capacity to acclimate varied dramatically among individuals. Some fish perfectly acclimated to the temperature change – the maximum swimming speed was the same at the two temperatures – while others could hardly adjust and thus performed much better at one temperature than the other. To understand why this variation exists, the authors first examined the possibility that acclimation ability negatively impacts maximum performance – the idea that a jack-of-all-trades is a master of none. For fish raised in warm water, the fastest swimmers were indeed those that had the lowest capacity to acclimate to cold conditions. Thus, the ability to adjust swimming physiology to changes in temperature comes at the expense of peak performance.
Next, the authors wanted to understand the mechanistic basis of this trade-off. They were particularly intrigued by the role of oxidative stress, which occurs when potentially damaging reactive oxygen species (sometimes called free radicals) form in the mitochondria as a by-product of energy production. Successful thermal acclimation depends on mitochondrial adjustments that often increase oxidative stress, and building cellular defence mechanisms to mitigate this stress is energetically costly. It is also well known that there are huge innate differences in the amount of oxidative stress experienced by individuals within a population. The authors thus reasoned that innately oxidatively stressed individuals might have less energy available for acclimation to changing temperatures. Consistent with this idea, mosquitofish with the smallest capacity for swim-performance acclimation also faced the highest levels of oxidative stress. Furthermore, this relationship between acclimation capacity and oxidative stress disappeared in mosquitofish that were experimentally administered the anti-oxidant drug N-acetylcysteine, suggesting a causal relationship between these variables.
Conventional wisdom states that the best way to cope with environmental change is to physiologically adjust in response. However, we now know that this is an energetically expensive solution that can limit maximum performance. To avoid this problem, mosquitofish seem to have evolved another solution to thrive in variable environments. These fish produce offspring that vary in the temperature at which they excel, ensuring that at least some individuals in the next generation will have the physiological tools required to do well in whatever the environment throws their way. And while this bet-hedging strategy may work well for mosquitofish, I'm sure glad my own parents took a different approach.
