Discussion
Parental age often has long-term consequences for offspring phenotype and fitness, but the mechanisms that mediate these effects remain insufficiently studied. Previous research suggests that telomeres may be an important mechanism mediating these effects, but the routes by which these effects occur are not well understood. The cross-fostering experiment used here allowed us to distinguish whether any effects of parental age on offspring telomeres occur as a result of epigenetic like and/or pre-natal effects vs. post-natal effects. Previous research in this colony of common gulls has demonstrated that offspring fitness decreases with increasing parental age: recruitment rate decreases in common gulls after the 10th breeding year (12-13 years of age) (Rattiste, 2004), and older gulls allocate less nutrients to their eggs (Urvik et al., 2018). However, despite these demonstrated effects of parental age on offspring fitness in this species, we did not find any evidence of the effect of parental age on offspring telomeres at hatching or the change in telomere length during post-natal development.
Although parental age has been shown to have both negative and positive effects on offspring telomere length (Table 4), this has not been found in all studies. For example, no effect of parental age on offspring telomere length was found in a study of Soay sheep (Ovis aries ) despite a large sample size (Froy et al., 2017). Although bird studies have generally found a negative effect of parental age on offspring telomeres (see for example studies in alpine swifts, (Criscuolo et al., 2017), and European shags Phalacrocorax aristotelis , (Heidinger et al., 2016), this is not a universal pattern (for example, older great reed warbles Acrocephalus arundinaceus produced offspring with longer telomeres, (Asghar et al., 2015b). Also in humans the effect of paternal age is positive rather than negative, as older fathers sire offspring with longer telomeres (Broer et al., 2013). A review article summarizing these results concluded that while there is no clear pattern across species, this is unlikely to be explained by statistical noise or publication bias (Eisenberg, 2014), but rather linked to the specific biology of each species. There are also several additional factors that could contribute to these mixed results: whether the study is experimental or correlative, at what age the offspring are sampled, and whether it is a longitudinal versus cross-sectional study of parental age. Accordingly, we cannot rule out that a longitudinal set-up would have revealed an effect of parental age on offspring telomere results also in our study system, as the cross-sectional design could have obscures the within individual patterns. Another possibility is that the link between parental age and offspirng telomere length in this species was too weak to be revealed from our sample size, despite relatively good test power (Table S3). In this case, and also in the case of a missing link, it is possible that telomere length in common gulls is indeed relatively buffered from environmental influence.
Telomere length was repeatable across the chick rearing period in our study, indicating a possible increase during post-natal development, and not being related to chick growth rate. Telomeres were longer at the second sampling, when chicks were approximately 11 days old. This period covered the fastest growth period of gull chicks. While telomeres shorten during growth in most studied adult vertebrates (which, as of now, mainly include mammals and some bird species), some vertebrates show increased telomerase activity during development (reviewed by Larsson, Rattiste, & Lilleleht, 1997, Monaghan & Haussmann, 2006). It has even been suggested that in free-living long-lived organisms, evolution should favour mechanisms that maintain the longest possible telomeres at the end of the most active growth period (Chan, & Blackburn, 2004). Studies in the wild have shown that telomeres elongate in at least some life stages in Seychelles warblers (Acrocephalus sechellensis (Spurgin et al., 2018)), edible dormouse (Glis glis(Hoelzl et al., 2016)), Soay sheep (Fairlie et al., 2016), Magellanic penguins (Spheniscus magellanicus (Cerchiara et al., 2017)), and Atlantic salmon (Salmo salar (McLennan et al., 2018)). However, when looking at the few studies on species more closely related to common gulls, telomere shortening during the early growth period has been reported. For example, in lesser black‐backed gull (Larus fuscus ), telomeres shortened from hatching to ten-days old (Foote et al., 2011), and in black-tailed gull chicks (Larus crassirostris ), telomere attrition was shown for chicks growing with siblings in the nest (but not singleton chicks (Mizutani, Niizuma, & Yoda, 2016)). The latter study suggests that, in favourable growing conditions, telomere attrition might be prevented. However, more results on closely related species are needed to confirm the possibility of telomere lengthening during early growth in gulls. Growth rate was independent of telomere length or telomere dynamics (Figure 3). In general, a trade-off between rapid growth and telomere maintenance is expected, due to increased number of cell divisions required to attain larger size, and/or increased loss of telomere length during each cell division as a consequence of the conditions required for fast growth (e.g. higher metabolic rate and ROS production reviewed by Monaghan & Ozanne (2018)). The current study adds to the increasing number of studies suggesting a different pattern in long-lived seabirds (Mizutani et al., 2016; Young et al., 2017). Seabirds are distinguished from most other species by a long time period between the end of relatively fast somatic growth and the beginning of reproduction (stretching several years). More studies applying comparable methodological approaches are needed for a comparative study, including patterns of growth and life-history strategies of different species to determine if this phenomenon of delayed reproduction is causally linked with the lack of an association between fast growth and telomere shortening in seabirds.
In conclusion, our results suggest that the age of the parents at the time of offspring conception does not influence offspring telomere length or the change in telomere length in common gulls. An important area of future research is to identify other mechanisms that mediate the long-term effects of parental age on offspring and to better understand the factors that contribute to the variation in the influence of parental age on offspring telomeres across species.