19The length of telomeres, the protective caps of chromosomes, is increasingly used as a biomarker 20 of individual health state since it has been shown to predict chances of survival in a range of 21 endothermic species including humans. Oxidative stress is presumed to be a major cause of 22 telomere shortening, but most evidence to date comes from in vitro cultured cells. The 23 importance of oxidative stress as a determinant of telomere shortening in vivo remains less clear 24 and has recently been questioned. 25We therefore reviewed correlative and experimental studies investigating the links between 26 oxidative stress and telomere shortening in vivo. While correlative studies provide equivocal 27 support for a connection between oxidative stress and telomere attrition (10/18 studies), most 28 experimental studies published so far (7/8 studies) partially or fully support this hypothesis. Yet, 29 this link seems to be tissue-dependent in some cases, or restricted to particular categories of 30 individual (e.g. sex-dependent) in other cases. 31More experimental studies, especially those decreasing antioxidant protection or increasing pro-32 oxidant generation, are required to further our understanding of the importance of oxidative 33 stress in determining telomere length in vivo. Studies comparing growing vs. adult individuals, or 34 proliferative vs. non-proliferative tissues would provide particularly important insights. 35 36
One of the reasons for animals not to grow as fast as they potentially could is that fast growth has been shown to be associated with reduced lifespan. However, we are still lacking a clear description of the reality of growth-dependent modulation of ageing mechanisms in wild animals. Using the particular growth trajectory of small king penguin chicks naturally exhibiting higher-than-normal growth rate to compensate for the winter break, we tested whether oxidative stress and telomere shortening are related to growth trajectories. Plasma antioxidant defences, oxidative damage levels and telomere length were measured at the beginning and at the end of the post-winter growth period in three groups of chicks (small chicks, which either passed away or survived the growth period, and large chicks). Small chicks that died early during the growth period had the highest level of oxidative damage and the shortest telomere lengths prior to death. Here, we show that small chicks that grew faster did it at the detriment of body maintenance mechanisms as shown by (i) higher oxidative damage and (ii) accelerated telomere loss. Our study provides the first evidence for a mechanistic link between growth and ageing rates under natural conditions.
BackgroundOne central concept in evolutionary ecology is that current and residual reproductive values are negatively linked by the so-called cost of reproduction. Previous studies examining the nature of this cost suggested a possible involvement of oxidative stress resulting from the imbalance between pro- and anti-oxidant processes. Still, data remain conflictory probably because, although oxidative damage increases during reproduction, high systemic levels of oxidative stress might also constrain parental investment in reproduction. Here, we investigated variation in oxidative balance (i.e. oxidative damage and antioxidant defences) over the course of reproduction by comparing female laboratory mice rearing or not pups.ResultsA significant increase in oxidative damage over time was only observed in females caring for offspring, whereas antioxidant defences increased over time regardless of reproductive status. Interestingly, oxidative damage measured prior to reproduction was negatively associated with litter size at birth (constraint), whereas damage measured after reproduction was positively related to litter size at weaning (cost).ConclusionsGlobally, our correlative results and the review of literature describing the links between reproduction and oxidative stress underline the importance of timing/dynamics when studying and interpreting oxidative balance in relation to reproduction. Our study highlights the duality (constraint and cost) of oxidative stress in life-history trade-offs, thus supporting the theory that oxidative stress plays a key role in life-history evolution.
Summary1. Life-history theory predicts that high reproductive investment alters self-maintenance. Several mechanisms underlying the cost of reproduction have been previously suggested, but how parental effort may impact cell and organism maintenance remains largely unknown. The effects of oxidative stress -the imbalance between oxidative damage and defences -on telomere dynamics may underlie this relationship. Indeed, oxidative stress is associated with costly activities like breeding, and impacts telomere length that is known to predict survival in birds. According to life-history theory, long-lived species are expected to minimize the adverse effects of current reproduction on their body maintenance and should therefore enhance their antioxidant capacity and preserve their telomeres when breeding workload increases. 2. In this study, we tested this hypothesis by determining experimentally how the oxidative status and telomere length were modified when long-lived Ade´lie penguins (Pygoscelis adeliae) faced a costly reproductive event. The breeding workload was increased through a handicapping procedure that increased the cost of foraging and therefore chick-provisioning. 3. In agreement with our hypothesis, Ade´lie penguins substantially increased their antioxidant defences during a costly breeding effort, while oxidative damage and telomere length remained unchanged. 4. As expected in long-lived species, Ade´lie penguins subjected to increased breeding constraints appear to prioritize self-maintenance as shown by their increased antioxidant capacity. Moreover, the absence of effects of our experimental procedure on telomere length suggests no apparent impact of breeding workload on the senescence of this long-lived bird. However, to better understand the role of the couple 'oxidative status ⁄ telomeres' in the regulation of life-history strategies, further studies should examine: (i) the nature and the cost of additional antioxidant protection; (ii) the changes in the oxidative status of animals throughout their annual cycle and the consequences on telomere dynamics; and (iii) the repartition of antioxidant resources between young and parents.
Telomeres are emerging as a biomarker for ageing and survival, and are likely important in shaping life-history trade-offs. In particular, telomere length with which one starts in life has been linked to lifelong survival, suggesting that early telomere dynamics are somehow related to life-history trajectories. This result highlights the importance of determining the extent to which telomere length is inherited, as a crucial factor determining early life telomere length. Given the scarcity of species for which telomere length inheritance has been studied, it is pressing to assess the generality of telomere length inheritance patterns. Further, information on how this pattern changes over the course of growth in individuals living under natural conditions should provide some insight on the extent to which environmental constraints also shape telomere dynamics. To fill this gap partly, we followed telomere inheritance in a population of king penguins (Aptenodytes patagonicus). We tested for paternal and maternal influence on chick initial telomere length (10 days old after hatching), and how these relationships changed with chick age (at 70, 200 and 300 days old). Based on a correlative approach, offspring telomere length was positively associated with maternal telomere length early in life (at 10 days old). However, this relationship was not significant at older ages. These data suggest that telomere length in birds is maternally inherited. Nonetheless, the influence of environmental conditions during growth remained an important factor shaping telomere length, as the maternal link disappeared with chicks' age.
Costs of reproduction can be divided in mandatory costs coming from physiological, metabolic, and anatomical changes required to sustain reproduction itself, and in investment-dependent costs that are likely to become apparent when reproductive efforts are exceeding what organisms were prepared to sustain. Interestingly, recent data showed that entering reproduction enhanced breeders' telomere loss, but no data explored so far the impact of reproductive investment. Telomeres protect the ends of eukaryote chromosomes. Shortened telomeres were associated with shorter lifespan, telomere erosion being then proposed to powerfully quantify life's insults. Here, we experimentally manipulated brood size in order to modify reproductive investment of adult zebra finches citation(Taeniopygia guttata) below or beyond their citation(optimal) starting investment and tested the consequences of our treatment on parents' telomere dynamics. We show that an increased brood size led to a reduction in telomere lengths in both parents compared to control and to parents raising a reduced brood. This greater telomere erosion was detected in parents immediately after the reproductive event and the telomere length difference persisted up to 1 year later. However, we did not detect any effects of brood size manipulation on annual survival of parents kept under laboratory conditions. In addition, telomere lengths at the end of reproduction were not associated with annual survival. Altogether, although our findings highlight that fast telomere erosion can come as a cost of brood size manipulation, they provide mixed correlative support to the emerging hypothesis that telomere erosion could account for the links between high reproductive investment and longevity.
Early-life adversity is associated with accelerated cellular ageing during development and increased inflammation during adulthood. However, human studies can only establish correlation, not causation, and existing experimental animal approaches alter multiple components of early-life adversity simultaneously. We developed a novel hand-rearing paradigm in European starling nestlings (Sturnus vulgaris), in which we separately manipulated nutritional shortfall and begging effort for a period of 10 days. The experimental treatments accelerated erythrocyte telomere attrition and increased DNA damage measured in the juvenile period. For telomere attrition, amount of food and begging effort exerted additive effects. Only the combination of low food amount and high begging effort increased DNA damage. We then measured two markers of inflammation, high-sensitivity C-reactive protein and interleukin-6, when the birds were adults. The experimental treatments affected both inflammatory markers, though the patterns were complex and different for each marker. The effect of the experimental treatments on adult interleukin-6 was partially mediated by increased juvenile DNA damage. Our results show that both nutritional input and begging effort in the nestling period affect cellular ageing and adult inflammation in the starling. However, the pattern of effects is different for different biomarkers measured at different time points.
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