INTRODUCTION
Telomeres, the nucleoprotein complexes involving tandem repeats of a
non-coding DNA sequence, prevent the ends of linear chromosomes from
inappropriately activating the DNA repair machinery (Blackburn, 1991).
In the absence of restoration, telomeres shorten with each cell division
due to incomplete replication of DNA at the chromosome ends, and their
eventual dysfunction limits cell replicative potential (Hayflick, 1965).
Telomeres may be further eroded by other processes including oxidative
damage (von Zglinicki, 2002; Reichert & Stier, 2017). Telomere length
(TL) changes might therefore reflect the cumulative costs associated
with acquiring and maintaining a particular body size, since this is
linked to cell replication levels (Monaghan & Ozanne, 2018), as
outlined in Fig. 1. The functional relationships between size, growth
and telomere dynamics might thus play an important role in shaping the
optimal body size in wild species under natural selection (Ringsby et
al. 2015; Erten & Kokko, 2020). Body size is a fundamental species
characteristic, which is intertwined with many aspects of species
ecology and evolution (Haldane, 1928; Peters, 1983; Woodward et al.,
2005; Sibly & Brown, 2007), and is under directional selection in many
species (Kingsolver & Pfennig, 2004). Both across and within species,
body size has been shown to correlate with important fitness-related
traits including survival, lifespan, fecundity and metabolic rate
(Bumpus, 1899; Gaillard et al., 1989; White et al., 2019). Life-history
theory predicts that organisms need to allocate their limited available
energy among different components of fitness, which leads to trade-offs
and selection for optimal solutions (Stearns, 1989). Trade-offs between
life-history traits may also occur due to antagonistic interactions; for
instance, if allocation of energy into developmental growth has negative
consequences due to long-term effects of telomere shortening (Fig. 1,
Monaghan et al., 2009; Young, 2018). For instance, Heidinger et al.
(2012) demonstrated a negative relationship between early-life TL and
lifespan in captive zebra finches (Taeniopygia guttata ). Negative
correlations between fitness-related traits may conform to the
hypothesized life-history trade-offs (Futuyma, 2010), but they are
difficult to observe in the wild, for instance due to variation among
individuals in resource acquisition (van Noordwijk and de Jong 1986) and
random environmental variation (Pujol et al., 2018). Nonetheless,
physiological or genetic constraints generating life-history trade-offs
may be detected by comparing different phenotypes or genotypes (Reznick,
1985), or through experimental manipulations involving for example
natural selection in a controlled environment or artificial selection in
the traditional breeder’s approach (Connor, 2003; Postma et al., 2007;
Pick et al., 2020). Correlated responses to artificial selection then
suggest additive genetic covariance between a trait and the selected
trait (Connor, 2003).
Several studies have investigated potential for telomere dynamics to
underpin individual variation in life-history strategies (Monaghan,
2010; 2014; Selman et al., 2012; Vedder et al., 2017). In the wild, many
of these studies, including long-lived bird species, mammals and
reptiles, suggest that most telomere loss occur during early life (Hall
et al., 2004; Spurgin et al., 2018) and that TL may be negatively
correlated with various developmental stress factors at this stage (Fig.
1), including brood competition (Boonekamp et al., 2014; Nettle et al.,
2016), poor nutrition and catch-up growth (Jennings et al., 1999; Geiger
et al., 2012). Such factors may result in the release of stress
hormones, which have been shown experimentally to increase early-life
telomere loss in the wild (Herborn et al., 2014), and oxidative stress
(Reichert & Stier, 2017) that may directly increase the shortening of
telomeres. In addition, body size has been shown to negatively correlate
with TL within different tetrapod species (Scott et al., 2006; Pauliny
et al., 2006; Debes et al., 2016; Caprioli et al., 2013; Ringsby et al.,
2015; Spurgin et al., 2018), which is thought to be due to the
additional number of cell divisions required for acquiring larger size,
and the increased oxidative stress associated with maintaining larger
size (Monaghan & Ozanne, 2018). The emerging field of telomere ecology
aims to identify factors that influence variation in individual TL and
their potential fitness consequences in free-living animals (Spurgin et
al., 2018). Whether there is a causal relationship between telomere
dynamics and individual variation in fitness in populations in the wild
and if TL is an indicator of individual quality are not yet fully
understood (Simons, 2015; Angelier et al., 2019). Experimental
approaches in both the field and the laboratory play an important role
in increasing our understanding of TL and life-history evolution.
In a large scale experimental study conducted in the wild, an artificial
directional selection regime on body size, as indicated by tarsus
length, was imposed annually and in opposite directions during four
consecutive years in two island populations of wild house sparrows
(Passer domesticus ) in northern Norway (Fig. 2). Each winter,
adult sparrows with tarsus lengths smaller or larger than given
thresholds were removed from each population to produce a significant
bidirectional change in mean tarsus length across the adult breeding
populations (Kvalnes et al., 2017). Relatively high heritabilities for
tarsus length have been found in these house sparrow populations
(h 2=0.3-0.4, Kvalnes et al., 2017), thus we
expected, based on the Breeder’s equation (Lande, 1979), the artificial
selection to result in significant responses in offspring tarsus lengths
and growth rates. Here, we initially show how the artificial selection
on parental tarsus length affected the size of their offspring measured
during the nestling stage. Tarsus length is commonly used as a proxy for
structural body size in house sparrows (Rising & Somers, 1989;
Araya-Ajoy et al. 2019). In a previous study based on a subsample of
chicks from the population undergoing artificial selection for larger
body size, Ringsby et al. (2015) showed that the selection regime had
indeed extended the range of chick body size at its upper end, and that
this was associated with a reduction in TL in red blood cells. In this
study, we examined whether the reciprocal effect, leading to longer TL,
occurred in the population in which body size was reduced, and also
examined the results in chicks whose parents were not subjected to the
selection regime. We constructed genetic pedigrees to identify nestlings
with parents that were subjected to artificial selection. We then
investigated how individual TL in nestling cohorts changed under the
different size selection regimes: We expected that increasing body size
through artificial selection led to shorter TLs through increased number
of cell divisions (Falconer et al., 1978) and oxidative stress
associated with increased energy expenditure (Geiger et al., 2012;
Pauliny et al. 2015; Smith et al., 2016; Monaghan & Ozanne, 2018).
Similarly, we expected that smaller body size and thus decreased
nestling growth led to a slower rate of TL reduction (Vedder et al.,
2018). Since TL was measured in early-life (fledgling stage) we also
examined environmental factors previously shown to influence telomere
loss during this period (Chatelain et al., 2020), specifically brood
competition (Boonekamp et al., 2014) and weather conditions (Graham et
al., 2019).
The artificial selection was expected to shift the populations away from
their optimal body size and increase the phenotypic variance across the
populations (Kvalnes et al., 2017). Here, we investigated whether
changes in TL following the artificial size selection might
mechanistically underpin fitness effects due to the deviation from the
optimal body size. Thus, the survival and reproduction of all
individuals on both islands were monitored during and after the
selection events. Hypothesizing that shorter TL relative to body size
would be associated with lower survival and reduced lifespan (Heidinger
et al., 2012), because short telomeres reflect adverse early-life
conditions (Wilbourn et al., 2018; Eastwood et al, 2019), we tested the
effect of TL on short-term (first-year) survival under the two selection
regimes, and on long-term survival (lifespan) after the artificial
selection events. Similarly, we tested if longer early-life TL predicted
higher future reproductive success (e.g. Pauliny et al., 2006; Olsson et
al., 2011; Heidinger et al., 2012; Bauch et al. 2013) and if any of the
potential trade-offs (Fig. 1) were affected by the artificial selection.