Discussion
Using longitudinal telomere measurements from the Lundy Island house
sparrow population, where precise ages, death status and reproductive
success are known, we estimated the relationships between telomere
dynamics and fitness measures, including survival and reproductive
success. We found that in post-fledging birds, independent of age,
longer telomeres were associated with higher chance to survive to the
next year. This finding was consistent with existing literature on adult
telomere length (e.g. Angelier et al., 2013; Barrett et al., 2013) and
meta-analytic results (Wilbourn et al., 2018). It also agrees with the
speculation of the selective disappearance of older birds with short
telomeres in the Lundy sparrows (Chik et al., 2023). The link between
telomere length and survival/mortality could be explained by two
mechanisms: Telomeres could play a causal and active role, by inducing
cell senescence and cell death at a critically short length. The
accumulation of senescent cells could hinder tissue functions, lead to
organ failure, and eventual death (Barrett et al., 2013; Monaghan, 2010;
Sahin et al., 2011). Alternatively, telomere length could also not
participate directly in causing death, but serve as an indicator of the
accumulative damage received by the body, or as a measure of ‘frailty’,
the capacity of the body to withstand and/or recover from damage
(Monaghan, 2010). Regardless of causality, our finding supports that
telomere length could serve as a biomarker of immediate survival.
Nevertheless, the demonstrated association between adult telomere length
and survival in our study contradicts others. In another insular house
sparrow study in Norway, authors found no correlation between early-life
telomere length and adult survival (Pepke et al., 2022). This could be a
result of habitat differences – in the Norwegian population, some
sparrows resided on islands with limited food and shelter, leading to
higher competition and increased juvenile mortality, ultimately the
decoupling of early-life telomere length and adult survival (Pepke et
al., 2022); whereas in the Lundy population, food and shelter is
available to sparrows year round, and mortality was less dependent on
resources availability and population density (Simons et al., 2019),
thus revealing a stronger effect of telomere length. As telomere
dynamics are influenced by environmentally-induced oxidative stress
(Monaghan & Ozanne, 2018), it is perhaps not surprising that the
telomere-mortality link would be context-dependant, necessitating
further studies using different ages, populations, and taxa (Wilbourn et
al., 2018).
Compared with survival, the link between telomere dynamics and lifespan
was much weaker, though still in the expected direction. This weaker
link could be the result of the more removed nature of lifespan as an
indicator of survival, or extrinsic factors. Independent of telomere
length, age was linked with mortality: the youngest and oldest birds had
a higher probability of dying. This could mean that other age-specific
factors, such as predation, became the main cause of death in the
shortest and longest living birds. This would weaken the link between
lifespan and telomere length at the extreme ages, and drive down sample
sizes, especially of long-lived birds, such that we could no longer
detect an effect of telomere length on lifespan. In the Lundy sparrows,
predation pressure was stronger in adults than in juveniles (Simons et
al., 2019), but we do not know the main cause of death in each age
class, nor have we tested for age dependency in TL-mortality
association. Further studies should address these topics. Nevertheless,
the effect found here agreed with the positive link we found between
telomere length and immediate survival.
If telomere length acts as an indicator of somatic redundancy/frailty,
then the TL-mortality link would be weaker at older ages, and the rate
of telomere shortening could emerge as a better predictor of lifespan
(Boonekamp et al., 2013; Monaghan, 2010). However, we did not find such
association here, as covariance between the rate of RTL change and
lifespan was not statistically significant, despite finding individual
variation in the rate of telomere shortening (Chik et al., 2023). This
could be a result of not having enough statistical power: In our
dataset, only 270 birds were sampled three times or more, and few
individuals lived to old ages of 9 and above.
In addition to survival, we also found a link between telomere length
and reproductive success, such that individuals with longer telomeres on
average, produce more genetic recruits over their lifetime, which in our
population, predicts expected genetic contribution and fitness (Alif et
al., 2022). In contrast, there was no evidence of any relationship
between annual telomere length and reproductive output. Our results
indicated that the link between telomere length and fitness is primarily
through higher survival, where individuals with longer telomeres survive
longer and as a result reproduced more, similar to the finding by
Heidinger et al. (2021), and consistent with the ‘individual quality
hypothesis’, i.e. individuals with a higher quality will have better
body conditions, and hence survival and/or reproductive prospects, than
poorer quality individuals, a trend found also in classical brood size
manipulation studies testing for survival-reproduction trade-offs
(Winder et al., 2022). One important contributor to variation in
individual quality is parental age at conception – previously we
detected such Lansing effect in the Lundy sparrows, where birds whose
biological parents were older when they hatched, produced fewer recruits
annually and over a lifetime, suggesting epigenetic detrimental effects
that were carried down generations (Schroeder et al., 2015). Further
studies should test for a similar Lansing effect in telomere dynamics to
better elucidate the intrinsic and extrinsic contributors to variation
in individual quality (e.g. Drake & Simons, 2023), and how telomere
dynamics is mechanistically linked to quality and reproduction.
In contrast, there was no relationship between annual telomere length
and reproductive output among individuals. This did not align with the
‘pace-of-life hypothesis’, under which individuals with a faster
pace-of-life are expected to sacrifice somatic maintenance for
reproduction, trading higher output for shorter telomeres. This could
mean that there is little variation in the pace-of-life in the Lundy
population, which is in line with another finding by Heidinger et al.
(2021). Alternatively, our result could also indicate that the
physiological costs of reproduction was not reflected on telomere
dynamics, or that the trade-off between reproduction and ageing is not
as strong within-species as previously considered, and masked by quality
effects (Winder et al., 2022). Indeed, we did not find an association
between the rate of telomere shortening and lifetime reproductive
output, nor a trade-off between telomere length and reproductive output
within an individual, suggesting that the lack of association could not
be attributed solely to differences in individual quality, e.g. in
resource acquisition or stress resistance. Note, however, that
reproductive success need not equate to reproductive effort. For
example, previous experiments have shown parents of enlarged broods had
shorter telomeres and faster shortening than those with unmanipulated or
reduced broods (Reichert et al., 2014; Sudyka et al., 2014). Further
studies should therefore examine the effect of e.g. parental care on
telomere dynamics, to determine whether the latter is an indicator of
the costs of reproduction in the Lundy sparrows.
In conclusion, in this study we examined the fitness consequences of
telomere dynamics in a longitudinal, closed house sparrow population,
and found evidence that indeed telomere length was correlated with
fitness. Our results provide additional support that telomere length is
linked with survival and therefore in turn with lifetime reproductive
success, but also add to the debate of the role of telomere shortening
as an indicator of senescence, somatic resilience, and fitness. It is
important as a next step to determine whether the associations we found
are only at the phenotypic level, or occur also at the genetic level,
which coupled with heritable variation in telomere dynamics (Chik et
al., 2023), would inform how telomere dynamics evolve in the wild.