Introduction
Parental age often has long-term effects on offspring phenotype in
humans (Carlaske, Tynelius, van den Berg, & Smith, 2019) and wild
animals (Bowers, Sakaluk, & Thompson, 2017). In some cases, parental
age has a positive long-term effects on offspring (Bradley & Safran,
2014), possibly because older parents are more experienced breeders than
younger parents and/or because reproductive investment increases with
age as future reproductive opportunities decline (e.g., terminal
investment) (Clutton-Brock, 1984). Alternatively, parental age may have
negative long-term effects on offspring if older parents experience
senescent declines in condition and/or reproductive function relative to
younger parents (Bock, Jarvis, Corey, Stone, & Gribble, 2019; Maklakov
& Chapman, 2019; Velarde & Menon, 2016). Regardless, the mechanisms
that underlie these long-term effects of parental age on offspring
phenotype are not well understood, although several candidate mechanisms
have been proposed, including, for example, epigenetic factors (Bock et
al. 2019).
One of the mechanism that has been proposed may mediate
trans-generational effects of parental on offspring fitness could be
offspring telomere length (TL). Telomeres are highly conserved,
repetitive, non-coding sequences of DNA that form protective caps at the
ends of chromosomes, thereby enhancing genome stability (Blackburn,
2005). While some evidence suggests that TL is largely inherited
(Blackburn, 2005), it is also known that TL and telomere dynamics are
affected by a complex interaction of genetic effects and environmental
factors during an organism’s life (Dugdale & Richardson, 2018;
Monaghan, 2010). While telomeres typically shorten with age in somatic
cells, elongation of telomeres has also been described, mainly as a
result of the activity of the enzyme telomerase, which can extend
telomeres via the addition of terminal telomeric repeats (Cong, Wright,
& Shay, 2002), and which is variably active in different cell types and
at different life stages (Gomes et al. 2011). The effect of parental age
on the length of offspring telomeres is currently an intensively studied
(e.g. Bauch, Boonekamp, Korsten, Mulder,& Verhulst, 2019; Criscuolo,
Zahn,& Bize, 2017; Heidinger et al. 2016; Froy et al. 2017; Noguera &
Velando, 2020). Costs and benefits associated with maintaining the
length of telomeres are particularly interesting when considering the
adaptive role of telomeres in the evolution of life histories, as it is
suggested that telomeres play a proximate causal role in current–future
life-history trade-offs (Young, 2018). Optimal life-history strategies
are both inherited and shaped by environmental effects (Stearns, 1992),
and accordingly, telomere dynamics are a plausible physiological
mechanisms related to life-histories (Giraudeau, Angelier, & Sepp,
2019).
While studies are accumulating that show parental age effects on
offspring telomeres, it is still unknown when these effects are
occuring. There are three potential routes through which parental age
could impact offspring telomeres (Haussmann & Heidinger 2015; Heidinger
& Young, 2020). First, age-associated changes in parental gametes may
affect the telomere length of offsprings. Parental age may negatively
influence offspring telomere length if older parents produce gametes
with shorter telomeres (shown for example in mice, Mus musculus ,
de Frutos et al. 2015), however, studies in humans have also shown that
older fathers may have offspring with longer telomeres (Broer et al.
2013; Unryn, Cook, & Riabowol, 2005), due to active telomerase in sperm
cells (Kimura et al., 2008). Such inconsistences among studies, but also
within species, could stem from differences in life-history strategies,
likely via mechanisms related to spermatogonial stem cell telomere
retention with increasing age, or selective attrition/survival of
spermatogonia (Kimura et al. 2008; Eisenberg & Kuzawa 2018). Studies in
humans have mostly found a link between paternal age and offspring
telomere length, however, the effect of maternal age has been shown to
be even stronger for some species (e.g. great reed warblerAcrocephalus arundinaceus , Asghar, Bensch, Tarka, Hansson, &
Hasselquist, 2015). While maternal reproductive cells develop at a very
early age, after which they are retained throughout life without further
cell divisions, association between mother age and offspring telomere
length could be explained by other mechanisms, for example age- and/or
condition-dependent telomerase activity in the ovaries (Asghar et al.
2015a; Kinugawa, Murakami, Okamura, & Yajima, 2000). Second possible
route is through pre-natal effects, for example age-associated changes
in the amounts of glucocorticoid or androgen hormones transferred from
the mother to the developing embryo with increasing age of the mother
(Haussmann & Heidinger, 2015; Heidinger & Young, 2020; Stier,
Metcalfe, & Monaghan 2019). This could in turn activate the production
of reactive oxygen species (ROS), as well as decrease telomerase
activity in the offspring (Haussmann & Heidinger, 2015), potentially
leading to telomere erosion. While there are now a number of studies
linking pre-natal stress to offspring telomeres (reviewed for example,
in Dantzer et al. 2020; Haussmann & Heidinger; 2015, Heidinger &
Young, 2020), none have included parental age in this equation. Third
route are post-natal effects, as age-related variation in parental care
and the characteristics of the post-birth environment could also be
important mediators of offspring telomere dynamic (Tarry-Adkins et al.
2009). For example, more experienced parents may provide better care
(Beamonte-Barrientos, Velando, Drummond, & Torres, 2010), but older
parents may also become less capable of providing a high quality
environment due to senescence effects (Torres, Drummond, & Velando,
2011). The quality of the parental care during the growth phase may
hasten or reduce telomere shortening (Criscuolo et al., 2017) with
long-lasting effects on the aging rate and life-history trajectories of
the organisms (Young 2018).
Distinguishing between the role of genetic/pre-natal and post-natal
effects on telomere length and telomere dynamics in natural populations
early in life is difficult, but potentially most important from an
evolutionary and ecological perspective (Dugdale & Richardson, 2018).
Birds are a promising model system for this kind of study, as the embryo
development takes place within a sealed system, the egg, limiting the
physiological maternal effects with the moment of egg laying.
Cross-fostering experiments are a useful tool, as they allow to tease
apart effects that are epigenetic and/or due to pre-natal egg effects,
from effects occuring during incubation and/or chick feeding. However,
to the best of our knowledge, there are only two studies that have used
cross-fostering approach to separate the genetic and environmental
effects of parental age on offspring telomere length. In alpine swifts
(Apus melba ), foster mother’s age negatively affected offspring
telomere length (Criscuolo et al., 2017). Bauch et al . (2019)
showed that paternal age effect on offspring telomere length is
independent of paternal care after conception in jackdaws (Corvus
monedula ). However, neither of these studies took repeated measures,
which are necessary to assess the change in TL and to separate
phenotypic variance into individual and residual variance components to
calculate repeatability (Stoffel, Nakagawa, & Schielzeth, 2017). In a
recent cross-fostering study of king penguins (Aptenodytes
patagonicus ), repeated measures of TL were taken, indicating that chick
telomere length was positively related to foster mothers’ TL at both 10
and 105 days after hatching, however, this study did not include
information about parental age (Viblanc et al 2020). Our study combines
both of these approaches, applying a cross-fostering manipulation
between differently aged parents with repeated measures of offspring
telomere length in a wild population of long-lived birds. We
cross-fostered whole clutches of common gull (Larus canus ) eggs
shortly after laying within and between age classes of young and old
parents, and assessed telomere length and dynamics during the chick
fastest growth phase. We predicted that if there are pre-natal,
epigenetic-like effects of parental age on offspring telomeres, there
will be a relationship between the age of the natal parent and offspring
telomeres, but if post-natal, environmental effects mediate the link
between parental age and offspring telomere length, there will be a
relationship between the age of the foster parent and offspring
telomeres.