DISCUSSION
In the last decade there has been an increasing interest in
understanding the ecological and physiological pathways affected by
extreme weather events, and their consequences for fitness (Thorntonet al. 2014). If there are critical windows in which telomere
dynamics are affected in a way that has lifelong effects, the timing of
these extreme weather events becomes very important. Our experimental
increase in nest temperature caused no overall change in telomere length
but does suggest that the pattern of consistent decline in telomere
length is altered in the chicks in the heat treated nests. While
telomeres of the control nestlings had a reduction, the experimental
group showed no changes during the first 12 days of life. This is
particularly important because diminished telomere shortening has been
highlighted as predictor of increased lifespan (Haussmann et al .
2003) and may reflect lower exposure to damage from ROS. Therefore, our
results match with our predictions and suggest that a warmer environment
during post-natal growth may produce transient benefits in 12 day old
ectothermic/poikilothermic nestlings.
The telomere dynamic we found between age 5 and 12 for heated nestlings
is consistent with other information generated in the same experimental
trial used in this study. Ton et al. (2021a) found no changes in
metabolic rates or growth caused by heat, and detected a lower body
temperature during the poikilothermic stage. The absence of acceleration
in growth and metabolic rates associated with lower body temperature is
expected to have no adverse consequences for stress and ROS production.
Indeed an increase in coupling activity during proton leak as found in
our previous study (Ton et al . 2021a) is hypothesized to reduce
costs from ROS (Brand 2000) that may be triggered independently from
variation in metabolic or growth rates; this could potentially prevent
oxidative damage to telomeres. Therefore, the absence of detrimental
treatment effects for telomeres that we detected here matches with
theoretical predictions generated from previous tests on the same
subjects (Ton et al. 2021a). Additionally, a recent study (in which
telomeres were not measured) indicated that moderate warming above
current temperature averages experienced during ontogeny and growth can
be beneficial by increasing the survival of ectothermic organisms, (Liuet al. 2022). Conversely, other studies documented detrimental
effects of heat waves (Zhang et al. 2018; Axelsson et al.2020), where lizards were exposed to stressful temperatures that
exceeded the field average by 6 oC had shorter
telomeres compared to those kept at cooler thermal conditions (Zhanget al. 2018). Our experiment involved much less severe heat
treatment, since we kept birds within ranges that reflect current
temperatures experienced in nature during their breeding season
(Griffith et al. 2016).
The effects of warming for telomere dynamics during some part of
nestling growth but not at other ages may be explained by the
thermoregulatory context. Nestlings are ectothermic initially after
hatching and gradually switch to endothermy (Sirsat et al. 2016),
when they can reach operational temperatures approaching 42C (McKechnie
& Wolf 2019). Our experiment suggests that bringing ambient
temperatures as close as possible to the physiological optima of
ectothermic nestlings (Friesen et al. 2021) provides some
resistance to the causes of telomere attrition. Of course it is possible
that other age-associated physiological changes may be involved, but
these findings are consistent with a study that demonstrated telomere
elongation in lizards kept at warmer temperatures (Fitzpatrick et
al. 2019) and longer telomeres in ectothermic organisms in the heat
(Burraco et al. 2020). This might also involve a higher
expression of telomerase, as predicted for ectotherms growing in warmer
environments (Olsson et al. 2018). Telomerase functions as a
repair mechanism for telomeres and shows higher activity during the
post-natal stage in ectothermic than in endothermic species (Olsson,
Wapstra, & Friesen, 2018). Our within species test show that
experimental heat waves reduced telomere attrition on chicks of zebra
finch during their ectothermic stage. However, post-natal stages of
songbirds that grow in enclosed or cavity nests are ectothermic only for
8-16 days in their life (Cheng & Martin 2012) and there may be
disagreement on whether they should be considered as a true ectotherm
during this short window. Still, the relationship between telomere
dynamics and heat waves during the first days after hatch aligns with
that found for true ectothermic species (Fitzpatrick et al. 2019;
Burraco et al. 2020). This result is particularly meaningful for
birds because, in contrast to other endothermic vertebrates, their
embryos grow outside of the stable thermal environment of the mother.
Indeed, early life stages of birds are subjected to considerable
temperature fluctuations due to variation in parental care (Martinet al. 2007), and this variation can have important downstream
consequences for development and metabolism (Ton & Martin 2017).
Here we also investigated the presence of complex strategies whereby
parent birds may buffer offspring to a degree in early life. We found
that our heat treatment significantly reduced brooding effort at the
nest. This is not a novel finding (Mitchell et al. 2020) but it
is important in the present context because a cross-fostering experiment
found parental care to drive telomere dynamics independently of genetic
background (Viblanc et al. 2020), and in that study, the role of
brooding behavior as a potential causal agent was not tested. The lower
rate of brooding we demonstrated for our heated nests have been
suggested to reflect energy benefits for the parents (Yom-Tov & Hilborn
1981; Bryan & Bryant 1999), but tests during incubation show that, as
temperature increases, these savings appear to be negligible (Tonet al. 2021b, Vleck 1981). Instead, lowering brooding at high
temperatures may be a strategy aimed at buffering potential risks of
thermal stress for the adults and for their offspring. However, we found
shorter telomeres associated to lower brooding effort for the heated
nestlings at age 12, which may reflect differences in parental quality
and heat tolerance. As already stated, the apparent effect of brooding
on telomere length that we detected needs to be interpreted with
caution, but encourages future studies to elucidate if lowering brooding
effort during extreme heat may yield higher chances of surviving and
therefore future reproduction for the parents, while also reducing
telomere length and future survival for the young.
Finally, we also found a negative correlation between telomere length
and body mass independently of treatment and age, and this is important
because both telomere and body size have been shown to be heritable
(Jensen et al. 2003; Boonekamp et al. 2020), and may
influence bird fitness (Ringsby et al. 2015). Similar results
were previously generated in a selection experiment aimed at
manipulating tarsus length which is related to structural size (Ringsbyet al. 2015), and in a descriptive study on the same species used
here (Sheldon et al. 2021). Similar to the findings of another
study (Boonekamp et al. 2020), variation in telomere length in
our analysis did not appear to be associated with differences in rates
of growth. This may be because in captivity with food available ad
libitum, all chicks were growing at their optimal rate and did not
experience the accelerated growth that is associated with higher
telomere attrition (Monaghan & Ozanne 2018).
Our study highlights the complexity of the mechanisms underlying
variation in telomere length by finding amelioration of telomere
attrition caused by heat during the ectothermic stage of an endothermic
species. This kind of effect has been found in other correlative and
experimental studies (Pipoly et al. 2013; Liu et al. 2022)
but the consequences for parental care and its potential contribution to
the thermal environment and to telomere dynamics and outcomes for
individuals over the life course is an avenue of research still in its
infancy that deserves further investigation.