10.5061/DRYAD.Z34TMPGF6
Wolf, Sarah
0000-0002-2620-8999
Indiana University Bloomington
Sanders, Tiana
Indiana University Bloomington
Beltran, Sol
Indiana University Bloomington
Rosvall, Kimberly
0000-0003-3766-9624
Indiana University Bloomington
The telomere regulatory gene POT1 responds to stress and predicts
performance in nature: implications for telomeres and life history
evolution
Dryad
dataset
2021
FOS: Biological sciences
protection of telomeres 1
bird
growth
recruitment
Lipopolysaccharide
Telomere
antioxidant
shelterin protein
early life
National Science Foundation
https://ror.org/021nxhr62
IOS-1656109
National Science Foundation
https://ror.org/021nxhr62
DBI-1460949
Eunice Kennedy Shriver National Institute of Child Health and Human Development
https://ror.org/04byxyr05
T32HD049336
2021-10-11T00:00:00Z
2021-10-11T00:00:00Z
en
https://doi.org/10.1101/2021.01.06.425609
99320 bytes
7
CC0 1.0 Universal (CC0 1.0) Public Domain Dedication
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.
We test the hypothesis that telomere regulatory mechanisms respond to
stress and predict performance in wild animals, evaluated with a focus on
POT1 ('protection of telomeres 1'). First, we ask whether POT1
gene expression is associated with three markers of individual quality in
breeding female tree swallows (Tachycineta bicolor), including first egg
date, body mass, and wing length (Winkler et al., 2020). We captured
females and measured their body mass and wing length when they were
rearing approx. 5-day old chicks. At the same time, we also collected
whole blood samples from each female for telomere length and POT1 gene
expression analyses. Second, we experimentally disrupted relationships
between POT1 and performance by exposing breeding females to an
ecologically relevant stressor (lipopolysaccharide injection), which leads
to ‘sickness’ in mothers, and 24h of food restriction in their offspring.
We assessed whether a female's telomere length and/or POT1 gene
expression predicted fluctuations in body mass and visitation rates
following injections. We also assessed effects of this stressor on their
offspring. We measured chick growth and key aspects of telomere biology
(i.e. change in relative telomere length, POT1 gene expression), as well
as other traits that have been linked to telomere dynamics in previous
work (i.e. glucocorticoids, antioxidants), mostly sampled one week after
maternal injections. Last, we recorded fledging success and recruitment of
chicks into the breeding population to assess whether telomere length
and/or POT1 gene expression predict survival-related metrics. Female
visitation rates: We quantified maternal visitation to the nest using PIT
tags and RFID readers positioned at the entrance of the nest box. Relative
telomere length: DNA was extracted from whole blood using a Promega
Maxwell RSC instrument, and telomere length was quantified using qPCR. For
questions relating to changes in chick telomere length over time, we use a
corrected metric accounting for initial telomere length at 5-days old
(corrected for regression to the mean). Gene expression: RNA was extracted
using a Trizol-based method. We then quantified antioxidant and POT1 gene
expression using qPCR. Corticosterone: We extracted hormone from plasma
using ether extractions and quantified CORT levels using an enzyme
immunoasssay kit (Cayman #501320). Datasets: The "FemaleRNA"
excel sheet is used to ask 1) whether female POT1 gene expression,
telomere length, and other variables predicts several metrics of quality,
and 2) whether POT1 and telomere length predict her responses to injection
with saline or LPS. The "ChickTelomereData" excel sheet is used
to ask 1) how chick phenotypes respond to maternal injections and 2)
whether chick phenotypes predict fledging success and recruitment into the
breeding population.
Please see the "Notes" tab on each excel datasheet for more
details about the columns/variables. Because of the nature of field work,
each variable of interest does have missing data for some individuals.
That information (# missing per variable and other subsetting) can be
found in the methods section of the published manuscript.