The telomere regulatory gene POT1 responds to stress and predicts performance in nature: implications for telomeres and life history evolution

Abstract

Long telomeres have become nearly synonymous with a variety of fitness-related traits and may be mediators of ecologically relevant variation in life history strategies. Growing evidence suggests that telomere dynamics are more predictive of performance than length itself, but very little work considers how telomere regulatory mechanisms respond to environmental challenges or influence performance in nature. Here, we combine observational and experimental datasets from free-living tree swallows (Tachycineta bicolor) to assess how performance is predicted by the telomere regulatory gene POT1, which encodes a shelterin protein that sterically blocks telomerase from repairing the telomere. First, we show that lower POT1 gene expression was associated with higher female quality, i.e. earlier breeding, and heavier body mass. We next challenged mothers with an immune stressor (lipopolysaccharide injection) that led to ‘sickness’ in mothers and 24h of food restriction in their offspring. While POT1 did not respond to maternal injection, females with lower constitutive gene expression were better able to maintain feeding rates following treatment. Maternal injection also generated a one-day stressor for chicks, who responded with decreased POT1 gene expression and elongated telomeres. Other putatively stress-responsive mechanisms (i.e. glucocorticoids, antioxidants) were not significantly different between control and stress-exposed chicks. Model comparisons indicated that POT1 mRNA abundance was a largely better predictor of performance than telomere dynamics, indicating that telomere regulators may be powerful modulators of variation in life history strategies.

A multi‐tissue view on telomere dynamics and postnatal growth

“…Furthermore, a mother's change in mass, but not her treatment, predicted nestling growth. This suggests that maternal LPS did not robustly manipulate resource availability across nests, in contrast to other work (Dantzer et al, 2008; Palacios et al, 2011; Wolf et al, 2021a). For blood telomere length, top models included treatment, but not maternal mass or nestling growth, suggesting that at least in this tissue, telomere maintenance responds more strongly to some unmeasured aspect of stress exposure as opposed to resource availability.…”

“…Conditional model averaging suggests that maternal LPS treatment led to shorter telomeres and higher rates of telomere attrition in nestling blood; however, full model averages do not, meaning the effect is weak. While significant decreases in blood telomere length have been shown at similar timescales in developing birds (Nettle et al, 2015; Stier et al, 2016; Wolf et al, 2021a), apparent telomere dynamics could also be driven by shifts in blood cell composition (Epel, 2012). Furthermore, a mother's change in mass, but not her treatment, predicted nestling growth.…”

“…We attempted to enhance variation in peak nestling growth via manipulations to maternal care using LPS, a nonreplicating piece of bacterial cell wall that temporarily triggers an immune response and induces “sickness” behaviors, e.g., lethargy, weight loss, and reduced parental care (Dantzer et al, 2008; Palacios et al, 2011; Wolf et al, 2021a). We administered a subcutaneous injection of either saline or LPS saline‐oil emulsion (0.4 mg/kg body weight) in the right dorsal apterium (saline: n = 14, LPS: n = 13).…”

“…We quantified telomere attrition in blood from 5 to 12 days old, as well as telomere length in 12-day-old blood, brain, adrenals, and liver. Importantly, past work suggests that telomere length can change within these several days (Nettle et al, 2015;Stier et al, 2016;Wolf et al, 2021a), especially during this period of incredible somatic growth. First, we assessed the directionality of growth-telomere relationships.…”

The telomere regulatory gene POT1 responds to stress and predicts performance in nature: Implications for telomeres and life history evolution

“…Data are available from the Dryad Digital Repository (https://doi.org/10.5061/dryad.z34tmpgf6) (Wolf, Sanders, et al, 2021).…”