Elevated reproduction does not affect telomere dynamics and oxidative stress

Abstract

Oxidative stress and telomere dynamics are considered to be powerful biomarkers quantifying a potential trade-off between current reproduction and self-maintenance. Recent studies confirmed the negative impact of elevated reproduction on telomeres, but the evidence for the cost of reproduction in terms of oxidative stress remains equivocal. In order to induce reproductive costs, we experimentally manipulated reproductive effort by increasing brood size in captive zebra finches (Taeniopygia guttata) and additionally challenged all birds by a low ambient temperature to facilitate detection of these costs. We were not able to show any negative effects of elevated reproductive effort on telomere dynamics and oxidative stress among parents, although brood enlargement was effective in terms of total mass and number of fledged young. Interestingly, irrespective of brood size treatment, we found a significant increase in antioxidant capacity at peak breeding while oxidative damage did not change with time. Our results may suggest that reproduction, instead of generating costs, may stimulate physiological functions promoting self-maintenance in terms of higher protection against free radicals. Possibly, opportunistic breeders such as zebra finches may not impede their future performance for the sake of current reproduction.Significance statementThis study interrogates a molecular background behind one of the most intriguing trade-offs that potentially occurs between self-maintenance and reproduction. We manipulated breeding effort in zebra finches to understand if the cost of reproduction can be mediated by telomere dynamics and oxidative stress. In our study system, we did not detect the direct reproductive costs in terms of parental oxidative damage and telomere loss; instead, these costs were paid by the offspring in terms of their inhibited growth rate. Moreover, we found that entering into the reproductive state strongly stimulated self-maintenance by increasing antioxidant capacity in parents. Our results emphasize that current reproductive success is not always prioritized over investment in body maintenance preventing the oxidative cost of reproduction.Electronic supplementary materialThe online version of this article (doi:10.1007/s00265-016-2226-8) contains supplementary material, which is available to authorized users.

Birds with high lifetime reproductive success experience increased telomere loss

“…As demonstrated in experimental studies [10,11], telomere shortening possibly reflects cumulative DNA damage caused by high reproductive effort. Elevated reproduction may cause telomere shortening owing to faster cellular turnover and overproduction of telomere-damaging free radicals by increasing metabolic rate ( [19,20], but see [21,22]), but also divert resources from telomere maintenance, i.e. telomerase activity or antioxidant protection [1,23].…”

Higher resting metabolic rate in long-lived breeding Ansell’s mole-rats (Fukomys anselli)

“…Especially in terms of female reproduction, a meta-analysis from different homeothermic vertebrates by Blount et al [ 8 ] has shown that in intraspecific comparisons between breeders and non-breeders, breeders had lower levels of oxidative damage in certain tissues. This effect could be attributed to upregulation of antioxidant defense mechanisms, such as glutathione or superoxide dismutase activity, which shows a tissue-dependent upregulation in several species during reproduction [ 36 – 39 ]. This oxidative shielding hypothesis, even if not consistent across different studies (reviewed in: [ 8 ]), suggests a reproduction-induced protection of mothers and offspring.…”

Does Physical Activity Age Wild Animals?

“…Unfortunately, few studies quantify the "effort" of the animals, for example in terms of their energy expenditure, and so are unable to show a link between effort and measures of senescence such as reduced survivability (though see: Daan et al, 1996). Moreover, there is only one study (and it is on captive animals-zebra finches), that includes measures of oxidative stress, DNA damage and survival (Sudyka et al, 2016). Hence, studies published so far investigating activity correlates of wild animal senescence have failed to combine all the following crucial elements: quantified physical activity, physiological and DNA damage, and measures of functional or demographic senescence.…”