The lingering impact of stress: brief acute glucocorticoid exposure has sustained, dose-dependent effects on reproduction

Abstract

Acutely stressful experiences can have profound and persistent effects on phenotype. Across taxa, individuals differ remarkably in their susceptibility to stress. However, the mechanistic causes of enduring stress effects, and of individual differences in stress susceptibility, are poorly understood. Here, we tested whether brief, acute increases in glucocorticoid hormones have persistent effects on phenotype, and whether effects differ according to the magnitude or duration of elevation. We used a novel method to non-invasively manipulate hormone levels on short time scales: the application of corticosterone gel to a model egg secured in the nest. Free-living female tree swallows (Tachycineta bicolor) exposed to several brief corticosterone increases during incubation showed dose-dependent differences in behaviour throughout the reproductive period. Birds receiving treatments that simulated higher or longer acute stress responses later provisioned larger broods at lower rates; the resulting offspring were smaller in size. Treatment did not influence female body condition, oxidative stress, reproductive success or inter-annual survival, but exposed females maintained higher baseline corticosterone after treatments ceased. Overall, these results indicate that brief, acute elevations in glucocorticoids in adulthood can have long-term consequences. Furthermore, individuals that mount a greater or longer acute stress response may be more likely to experience lingering effects of stress.

Keywords: carry-over effect; corticosterone; fitness; life-history trade-off; oxidative stress; parental behaviour.

Figure 1.

Immediate effects of corticosterone manipulation. Box-plots illustrate the mean and IQR and whiskers represent the range of natural variation in baseline (n = 360) and stress-induced corticosterone (n = 366; following 30 min of standardized restraint stress) in tree swallows in this population. Green arrows illustrate when doses (corticosterone + DMSO or DMSO only) were placed on model eggs. Coloured lines represent mean (±s.e.) corticosterone levels in birds sampled 30, 90 or 180 min after the first dose (n = 69); circles illustrate individual sample concentrations [30]. Asterisks represent significant differences between the control and treatment groups in post hoc tests (*p < 0.05, **p < 0.01).

Figure 2.

Daily time at nest entrance during incubation. Half violin plots show raw data on the left, and the model predicted mean and confidence interval for each treatment group on the right.

Figure 3.

Effects of treatment on offspring provisioning rate. Curves show model predicted relationships (n = 9391 measures of hourly provisioning; 45 females). To illustrate the interaction between treatment and brood size, the relationship is plotted for broods with (a) three nestlings and (b) six nestlings. Hour, ambient temperature and clutch initiation date are held at their average values. The shaded region around each line represents the confidence interval. The vertical dashed line indicates the day of nestling phenotype measurement.

Figure 4.

Effects of treatment on offspring phenotype. Lines illustrate model predicted relationships between brood size and (a) nestling body mass and (b) wing length across treatment groups (n = 208; control n = 43, vehicle control n = 33, low n = 51, high n = 42, long n = 39). Clutch initiation date and ambient temperature are held at their average values. Coloured circles represent the treatment mean and standard error for each brood size.