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

Telomeres are emerging as correlates of fitness-related traits and may be
important mediators of ecologically relevant variation in life history
strategies. Growing evidence suggests that telomere dynamics can be 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 POT1 gene expression were better able to maintain feeding
rates following treatment. Maternal injection also generated a one-day
stressor for chicks, which responded with lower POT1 gene expression and
elongated telomeres. Other putatively stress-responsive mechanisms (i.e.
glucocorticoids, antioxidants) showed marginal responses in 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.