The hypothesized negative relationship between growth rate and lifespan has proved very difficult to test robustly because of potentially confounding variables, particularly nutrient availability and final size. Here we provide, to our knowledge, the first rigorous experimental test of this hypothesis, and find dramatic changes in lifespan in the predicted direction in response to both upward and downward manipulations of growth rates. We used brief (less than 4% of median lifespan) exposure to relatively cold or warm temperatures early in life to deflect juvenile three-spined sticklebacks Gasterosteus aculeatus from their normal growth trajectories; this induced catch-up or slowed-down growth when ambient temperatures were restored, and all groups attained the same average adult size. Catch-up growth led to a reduction in median lifespan of 14.5 per cent, while slowed-down growth extended lifespan by 30.6 per cent. These lifespan effects were independent of eventual size attained or reproductive investment in adult life. Photoperiod manipulations showed that the effects of compensatory growth on lifespan were also influenced by time available for growth prior to breeding, being more extreme when less time was available. These results demonstrate the growth-lifespan trade-off. While growing more slowly can increase longevity, the optimal resolution of the growth-lifespan trade-off is influenced by time constraints in a seasonal environment.

Early environmental conditions can influence the pattern of growth and development. While poor conditions generally cause slower growth, normal adult size can still be reached if growth accelerates or is prolonged once conditions improve, but such catch-up growth may have deleterious effects later in life. Here we investigate for the first time how decelerating as well as accelerating growth trajectories, manipulated independently of food supply, affect subsequent breeding performance. In order to alter growth rates we subjected juvenile three-spined sticklebacks Gasterosteus aculeatus to a short period of altered environmental temperature (high, intermediate, or low), after which all fish had the same (intermediate) temperature regime. In addition, the perceived time stress (until the onset of the spawning season) was manipulated by conducting the experiment twice (in the winter and in the spring immediately prior to breeding) and by exposing half of the fish in each experiment to a delayed photoperiod (two months behind ambient). We found that fish showed full growth compensation, such that in all treatments they were of the same average size by the start of the breeding season. However, those compensating for low temperatures earlier in life (i.e., who then showed an accelerated growth trajectory) had reduced reproductive investment over the following two breeding seasons (males, reduced sexual ornaments and speed of building nests; females, reduced first clutch size, mean egg size, and eggs produced per year). Moreover, these deleterious effects were strongest when the perceived time available for growth compensation prior to breeding was shortest. In contrast, those fish with a decelerating growth trajectory as a result of exposure to high temperatures early in life showed an improved breeding performance compared to steadily growing controls. These results clearly demonstrate that both the shape of the growth trajectory (independent of food supply) and the time available for growth compensation have broad-reaching and prolonged effects on breeding performance, with ecological conditions that prompt catch-up growth just prior to the breeding season being especially damaging for both sexes.

SUMMARYEnvironmental circumstances can cause changes in early growth patterns that subsequently affect the adult phenotype. Here we investigated how different growth trajectories affected subsequent locomotor performance, and how such effects were influenced by the perceived time until the key life-history event of reproduction. Using juvenile three-spined sticklebacks Gasterosteus aculeatus, we show that a brief period of manipulated temperature in early life (independent of food supply) caused effects on skeletal growth trajectory not only during the manipulation itself, but also during a subsequent compensatory phase. The outcome of these changes was that fish in all treatment groups reached the same average size by sexual maturity, despite having different growth patterns. However, their growth trajectory had impacts on both pre-breeding swimming endurance and its decline over the course of the breeding season, such that swimming ability was negatively correlated with skeletal growth rate during the compensation period. We also show for the first time that 'negative compensation' (i.e. a decelerating growth trajectory) led to an improved swimming performance compared with steadily growing controls. Replicate experiments and photoperiod manipulations, moreover, revealed that the effects of growth rate on subsequent swimming performance were greater when the perceived time until the breeding season was shorter. These results show that the costs of accelerated or decelerated growth can last well beyond the time over which growth rates differ, and are affected by the time available until an approaching life history event such as reproduction, possibly because of the time available to repair the damage.

Fast growth can be costly, so trade-offs between growth and fitness are to be predicted when organisms adjust their growth to compensate for earlier environmental conditions. We developed four generic models of increasing complexity with different processes to predict the indeterminate growth of vertebrate ectotherms, which is sensitive to ambient temperature even when food is not limiting. We contrast the predictions of the models with observed experimental data on growth trajectories, feeding activity, and reproductive investment of three-spined sticklebacks and inferred patterns of accumulation of biomolecular damage arising from activity and growth. All models predicted observed patterns of compensatory growth (both accelerating and decelerating) in response to earlier temperature perturbations, but the more complex models provided the best fit to experimental data. Growth trajectories influenced future reproductive investment regardless of final body size at breeding. Our findings suggest that while models with fewer parameters can predict basic patterns of growth in stable conditions, they cannot capture the costly long-term effects of deviations from steady growth trajectories. In contrast, models in which foraging activity is assumed to carry costs are capable of predicting the complex patterns of feeding, growth, and reproductive investment seen in animals, with the cost of a heightened mortality risk (e.g., through predation) being more important than the cost of increased physiological damage.