Developmental telomere attrition predicts impulsive decision-making in adult starlings

Abstract

Animals in a poor biological state face reduced life expectancy, and as a consequence should make decisions that prioritize immediate survival and reproduction over long-term benefits. We tested the prediction that if, as has been suggested, developmental telomere attrition is a biomarker of state and future life expectancy, then individuals who have undergone greater developmental telomere attrition should display greater choice impulsivity as adults. We measured impulsive decision-making in a cohort of European starlings (Sturnus vulgaris) in which we had previously manipulated developmental telomere attrition by cross-fostering sibling chicks into broods of different sizes. We show that as predicted by state-dependent optimality models, individuals who had sustained greater developmental telomere attrition and who had shorter current telomeres made more impulsive foraging decisions as adults, valuing smaller, sooner food rewards more highly than birds with less attrition and longer telomeres. Our findings shed light on the biological embedding of early adversity and support a functional explanation for its consequences that could be applicable to other species, including humans.

Keywords: European starling; body condition; impulsivity; self-control; state-dependent decision-making; telomere dynamics.

Figure 1.

(a) Brood size manipulation. The diagram shows the creation of a single family of four focal chicks. A total of eight such families were created, yielding 32 focal chicks. (b) Inter-temporal choice task. The format of a single choice trial is shown. All trials began with an amber initiation light. One coloured key (here green) was assigned to the smaller sooner option (a 1 s delay to obtain one 45 mg pellet), and the other colour (here red) was assigned to the larger later option a longer, x s delay to obtain five 45 mg pellets). (Online version in colour.)

Figure 2.

Telomere dynamics. (a) Having more, heavier competitors on d15 predicts greater developmental telomere attrition between d4 and d55. Telomere attrition is measured by D [22]; positive values of D indicate telomere lengthening over development and negative values indicate telomere loss. The solid black line is the line of best fit from a simple linear regression model, with 95% CIs shaded in grey. (b) Correlation between telomere length at d55 and telomere length at 14 months. The units of measurement are T/S ratios. The solid line shows the expectation if there was no change in telomere length. (c) Greater developmental telomere attrition (D) predicts shorter telomere length (T/S ratios) at 14 months. The graphs show data from all 23 birds for which we had telomere length measurements; the three birds lacking behavioural data are indicated with open circles.

Figure 3.

Estimates of choice impulsivity for individual starlings. Data are estimates of k for the 28 birds for which we obtained behavioural data. Birds are grouped by genetic family and the dashed line shows the mean value of k obtained. The shaded zones show the ranges of k reported in the literature for rats and pigeons.

Figure 4.

Predictors of impulsivity. (a) Greater developmental telomere attrition (D) predicts greater impulsivity. (b) Poorer body condition predicts greater impulsivity. In both panels, the data points represent the subset of 20 birds for which we obtained both developmental telomere lengths and estimates of impulsivity. The solid black line is the line of best fit from a simple linear regression model, with 95% CIs shaded in grey.