14.9 THIS IS HOW WE DO IT: Life history trade-offs: rapid growth comes at a cost.

Sometimes it’s tricky to collect experimental evidence supporting a theoretical prediction, even when it seems extremely likely that the prediction is accurate. This is the case for the idea that there must be a trade-off between growth and longevity.

Collecting the appropriate evidence is challenging due to several confounding factors.

1. If you look at the slowest-growing organisms in a population, they may turn out not to have the greatest longevity simply because their slow growth is due to poor nutrition—which tends to reduce longevity.

2. If you look at the fastest-growing organisms, they may have the greatest longevity simply because their faster growth reflects access to better nutrition.

3. And, because growth rate is often positively correlated with adult body size—which is, in turn, positively correlated with longevity—the fastest-growing organisms may end up having the greatest longevity.

In each of these cases, the data aren’t appropriate for evaluating whether there is a trade-off specifically between growth and longevity. Testing that prediction requires extremely well-controlled experiments.

In a 2013 paper in the Proceedings of the Royal Society of London, some researchers reported a clever experimental approach that enabled them to evaluate, in a rigorous way and for the first time, the relationship between growth rate and life span. Here’s how they did it.

Working with small (∼5 cm long) fish called three-spined sticklebacks (Gasterosteus aculeatus), the researchers were able to alter the growth trajectories of the fish by manipulating the temperature of their aquarium water. The sticklebacks are ectothermic, meaning that, unlike us, they don’t maintain a constant body temperature. Rather, their body temperature decreases or increases with the temperature of the water in which they are living.

The researchers randomly assigned groups of fish to one of three temperature conditions: normal (6° C), warmer (10° C), or cooler (4° C). They maintained them at this temperature for 4 weeks, designating this as Period 1. All of the groups were then maintained at 6° C (normal temperature) for the remainder of the fishes’ lives, designated Period 2. Because the median life span of these sticklebacks is about two years—with many living three years or longer—Period 1 represented less than 4% of the median life span.

The effect of the temperature manipulation was to reduce growth at the cooler temperature and increase growth at the warmer temperature during Period 1. As expected, at the end of this period there were significant differences in the average size of the sticklebacks in the three experimental groups.

The temperature perturbations, however, had another effect: they altered growth rates during Period 2, when all were kept at the normal temperature of their environment. Sticklebacks from the populations maintained at a cooler temperature in Period 1 (which had grown more slowly) experienced more rapid, “catch-up” growth, and those maintained at a warmer temperature in Period 1 exhibited slowed-down growth. As a result of the catch-up or slowed-down growth, after 3–4 months there were no differences among the three groups in the average size of the fish.

As noted above, the researchers maintained all of the sticklebacks until they died, and they monitored their longevity. When they compared the average life spans across the three groups, the results were dramatic.

• Groups that spent Period 2 in catch-up growth had a decreased median life span—14.5% lower than that of the normal-temperature group.
• Groups that spent Period 2 in slowed-down growth had an increased life span—30.6% higher than that of the normal-temperature fish.

The researchers concluded that the results demonstrated the existence of a growth–life span trade-off.

They also reported additional measurements that supported their conclusion and provided evidence that the experiment was very well-controlled. The life span differences were independent of (1) the eventual size attained by the fish, and (2) the reproductive investment made by the fish during Period 2. Also, life span was unrelated to growth rate during the temperature manipulation (Period 1).

In discussing their results, the researchers noted that the sticklebacks grew more quickly or slowly during Period 1 as a consequence of digesting and processing food more quickly or slowly. And that depended solely on the temperature. Why didn’t this affect longevity? Because the differences in growth rate were not a consequence of diverting resources away from maintaining their bodies.

During Period 2, however, all the fish were living at the same temperature, so those growing more slowly were able to divert more resources to maintenance or reproduction. Those growing more quickly, on the other hand, could achieve that increased growth only by diverting valuable resources away from maintenance and reproduction.

The experimental design did not allow the researchers to determine the mechanisms for the longevity differences. They speculated, however, that more rapid growth during Period 2 may have led to more cellular damage, resulting from stresses associated with increased metabolic activity.