Introduction
Understanding how an organism’s fitness is influenced by its traits is a
central tenet in evolutionary biology. While most measurable traits are
manifested at the organismal level, for example in reproduction,
survival, and behaviour, it is equally important to examine traits at
deeper levels of biological organization, including cell and body
physiology, as they underlie organismal performance. One of such traits
is telomere dynamics, which could reflect the cellular and body state of
the organism, bridging together physiology and fitness.
Telomeres are nucleoprotein complexes at the ends of chromosome
consisting of repeating DNA sequences (TTAGGGn in
vertebrates; Blackburn, 1991). Telomeres are vulnerable to erosion due
to 1) the end-replication problem, where linear DNA is not fully
replicated during cell proliferation (Levy et al., 1992; Olovnikov,
1973); and 2) chemical damage from oxidative stress (Blackburn et al.,
2015; von Zglinicki, 2002). They therefore shorten over time. Shortened
telomeres can be restored, e.g. by telomerase, but telomerase activity
varies across life stages and species (Haussmann et al., 2007), and is
generally thought to be suppressed in adult somatic cells in humans and
mammals (Blackburn et al., 2015; Young, 2018). This creates a decline of
telomere length throughout lifespan, typically rapidly during early life
due to prominent cell proliferation, and more slowly in adulthood
(Heidinger et al., 2012; Spurgin et al., 2018; Stier et al., 2020),
though patterns vary across taxa (Remot et al., 2022). When telomeres
are critically short, cells enter a senescent state, and can undergo
apoptosis, leading to a decline in tissue function (Blackburn et al.,
2015; Campisi, 2005). Because of this, telomere length, and the rate of
telomere shortening, have gained attention in evolutionary biology and
epidemiology, as a biomarker of body state or individual quality (e.g.
Angelier et al., 2019; Bauch et al., 2013; Monaghan, 2010), a
measurement of physiological costs in life-history trade-offs (e.g.
Bauch et al., 2013), and a hallmark of ageing (e.g. López-Otín et al.,
2013).
Because telomeres link to cellular senescence, thereby tissue function,
and thus perhaps ultimately ageing, one would expect telomere dynamics
to be under selection, and therefore to be correlated with fitness.
However, studies examining the relationship between telomere dynamics
and survival and/or lifespan have provided mixed results. On average,
shorter telomeres are associated with higher mortality, but variation
exists (Wilbourn et al., 2018). Some studies found positive
relationships between early-life telomere length and survival or
lifespan (e.g. Eastwood et al., 2019; Fairlie et al., 2016; Heidinger et
al., 2012; Sheldon et al., 2022; van Lieshout et al., 2019); while
others found such a relationship also in adults (e.g. Bakaysa et al.,
2007; Bichet et al., 2020; Froy et al., 2021; Vedder et al., 2022), even
at a genetic level (Vedder et al., 2022). There has also been some
evidence that telomere shortening predicts survival and/or lifespan
(e.g. Boonekamp et al., 2014; Brown et al., 2022; Tricola et al., 2018;
Whittemore et al., 2019; Wood & Young, 2019). To date, it remains
unclear whether, and how, telomere biology causally contribute to
organismal senescence (Simons, 2015; Young, 2018) and fitness variation.
This is particularly true for adult telomere dynamics, as most studies
focused on early-life telomere lengths.
The link between telomere dynamics and reproductive success, another
essential component of fitness, also demands attention (Sudyka, 2019).
Two main hypotheses link telomere dynamics with variation in
reproductive output: (1) the ‘individual quality hypothesis’ suggests
that individuals with longer telomeres and/or slower telomere shortening
are of higher quality, either due to genetic differences (e.g. Pepke et
al., 2023), or environmental variation, e.g. better habitat that offers
more resources and less stress, such that these individuals both live
longer and have higher lifetime and annual reproductive output,
generating a positive relationship between telomere dynamics and
reproduction (e.g. Angelier et al., 2019; Heidinger et al., 2021). (2)
The ‘pace-of-life hypothesis’ suggests that individuals differ in their
relative energetic investment in self maintenance versus reproductive
effort, such that individuals with a slower pace-of-life would exhibit a
longer lifespan, have longer telomeres and slower shortening, but
decreased annual reproductive success, resulting in a negative
relationship between telomere dynamics and reproduction (Bauch et al.,
2020; Bichet et al., 2020; Eastwood et al., 2019; Heidinger et al.,
2021; Ravindran et al., 2022). So far, research has largely focused on
early-life telomere length and its association with reproductive output,
and has provided mixed results: Support for the ‘individual quality
hypothesis’ was found by e.g. Angelier et al., (2019); Eastwood et al.,
(2019) and Heidinger et al., (2021), whereas support for the
‘pace-of-life hypothesis’ was found by e.g. Bauch et al., (2013) and
Pepke et al., (2022). Additionally, it is still unclear how telomere
shortening relates to reproductive output. For example, Heidinger et al.
(2021) did not find an association between telomere shortening and
reproductive success, while Sudyka et al. (2019) found a negative
association. Further testing for fitness associations with telomere
length and shortening, especially in longitudinal, natural systems, can
thus enable us to better understand the evolutionary mechanism that
drives variation in telomere dynamics.
Here, we examined the links between telomere dynamics and fitness in a
free-living, insular population of house sparrows (Passer
domesticus ), using longitudinal telomere measurements that span 16
years, and for which we have precise survival and lifetime reproductive
data. As there has been a relative lack of focus on telomere dynamics
beyond early life, we selected samples and quantified telomere lengths
from birds after they have fledged, and tested: 1) whether adult
telomere length predicts immediate survival up to 1 year
post-measurement; 2) whether average individual telomere length and rate
of telomere shortening across adulthood are associated with lifespan; 3)
whether adult telomere length is associated with annual reproductive
output; and 4) whether average telomere length and telomere shortening
are associated with lifetime reproductive output.