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.