The trade-off between growth rate and locomotor performance varies with perceived time until breeding

Abstract

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.

Experimental demonstration of the growth rate–lifespan trade-off

“…As a result of the treatment differences in compensation, the size of the fish within each experiment converged; the significant length differences among temperature-treatment groups found at the end of period 1 had disappeared after 15 weeks at the ambient temperature in the winter experiment and after 12 weeks in the spring experiment (figure 1). While there was no overall effect of photoperiod treatment on compensatory growth rate ( 23, p , 0.001) influenced compensatory growth: males grew slower than females, and growth rate was faster in fish that were smaller at the end of the temperature manipulation period (see [11,12] for more detailed statistical analysis).…”

“…We randomly allocated the four replicate tanks of five fish to each of these manipulation groups in both experiments; the analyses in this study are therefore based on a total initial sample size of 240 fish. Details of the effects of the treatments on the swimming and breeding performance of the same fish are given in [11,12], respectively; here we examine the effects on lifespan.…”

“…If this is so, the consequences of any changes in growth rate should also be influenced by the degree of time stress under which they occur. Recent experimental results provide some support for this hypothesis: animals given a shorter time period over which to attain a target size prior to reproduction showed reduced starvation resistance, poorer locomotor and breeding performance [9,11,12]. However, it is not known whether time-stress influences any effects of growth rate on potential lifespan.…”

“…The degree of perceived time stress can be altered by using shifted photoperiod regimes [12]. By using both temperature and photoperiod manipulations, we examined here: (i) how perturbations of growth trajectories affect lifespan, and (ii) whether such effects are influenced by time stress.…”

“…Thus, the rate of catch-up growth and/or the subsequent cost to lifespan should be greater when there is a shorter period of time available to compensate prior to the breeding season. Since our predictions relate to the direct effects of growth rate on lifespan, and since the manipulations had no effect on final adult size [12], we expected that the growthlifespan interrelationships would be independent of any indirect consequences for lifespan that come about through effects of growth rate on reproductive investment or adult body size.…”