Magellanic penguin telomeres do not shorten with age with increased reproductive effort, investment, and basal corticosterone

Abstract

All species should invest in systems that enhance longevity; however, a fundamental adult life‐history trade‐off exists between the metabolic resources allocated to maintenance and those allocated to reproduction. Long‐lived species will invest more in reproduction than in somatic maintenance as they age. We investigated this trade‐off by analyzing correlations among telomere length, reproductive effort and output, and basal corticosterone in Magellanic penguins (Spheniscus magellanicus). Telomeres shorten with age in most species studied to date, and may affect adult survival. High basal corticosterone is indicative of stressful conditions. Corticosterone, and stress, has been linked to telomere shortening in other species. Magellanic penguins are a particularly good model organism for this question as they are an unusually long‐lived species, exceeding their mass‐adjusted predicted lifespan by 26%. Contrary to our hypothesis, we found adults aged 5 years to over 24 years of age had similar telomere lengths. Telomeres of adults did not shorten over a 3‐year period, regardless of the age of the individual. Neither telomere length, nor the rate at which the telomeres changed over these 3 years, correlated with breeding frequency or investment. Older females also produced larger volume clutches until approximately 15 years old and larger eggs produced heavier fledglings. Furthermore, reproductive success (chicks fledged/eggs laid) is maintained as females aged. Basal corticosterone, however, was not correlated with telomere length in adults and suggests that low basal corticosterone may play a role in the telomere maintenance we observed. Basal corticosterone also declined during the breeding season and was positively correlated with the age of adult penguins. This higher basal corticosterone in older individuals, and consistent reproductive success, supports the prediction that Magellanic penguins invest more in reproduction as they age. Our results demonstrate that telomere maintenance may be a component of longevity even with increased reproductive effort, investment, and basal corticosterone.

Early‐breeding females experience greater telomere loss

“…For example, breeding zebra finches (Taeniopygia guttata) exhibited higher telomere loss compared to nonreproductive individuals, but the number of reproductive bouts in breeding birds was not correlated with telomere length (Heidinger et al, 2012). The lack of a relationship between annual change in telomere length and reproductive performance is additionally supported by a recent study in Magellanic penguins (Spheniscus magellanicus) (Cerchiara et al, 2017). Our finding that cooler temperatures are correlated with telomere shortening could instead suggest that the conditions experienced during reproduction affect telomere dynamics more strongly than the total number of offspring produced by female passerines within a season.…”

Sex‐biased survival contributes to population decline in a long‐lived seabird, the Magellanic Penguin

“…In Wandering Albatross, the foraging skills of fledglings improve rapidly over the first few months at sea, after which they are comparable to those of adults (Weimerskirch 2018). We found that survival decreased again for individuals ≥19 yr of age, potentially because of senescence-related reductions in foraging efficiency (e.g., Zimmer et al 2011) or to increased investment in reproduction with age (Cerchiara et al 2017). Interestingly, Rebstock and Boersma (2018) found that egg size increased with female Magellanic Penguin age until age 18 and then began to decline, another indication that senescence begins around age 19 in females of this species.…”

“…) or to increased investment in reproduction with age (Cerchiara et al. ). Interestingly, Rebstock and Boersma () found that egg size increased with female Magellanic Penguin age until age 18 and then began to decline, another indication that senescence begins around age 19 in females of this species.…”

On the evolution of cellular senescence

“…If replicative senescence acts as an anti-cancer mechanism by limiting the number of possible cell divisions, it seems that the actual rate of telomere loss is of greater relevance than raw telomerase activity, since reactive oxygen species and various stressful conditions can influence the rate of shortening (Cerchiara et al, 2017;von Zglinicki et al, 1995). Indeed it has been shown that DNA damage limits the division potential of mouse fibroblasts under standard culture conditions (20% O 2 ), while they reach more than 60 population doublings when kept under 3% oxygen (Parrinello et al, 2003), which is in agreement with the fact that mice have long telomeres and express telomerase.…”