Elevated reproduction does not affect telomere dynamics and oxidative stress

Sudyka, Joanna; Casasole, Giulia; Rutkowska, Joanna; Cichoń, Mariusz

doi:10.1007/s00265-016-2226-8

Cited by 17 publications

(17 citation statements)

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“…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].…”

Section: Resultsmentioning

confidence: 99%

Birds with high lifetime reproductive success experience increased telomere loss

et al. 2019

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Lifetime reproductive success (LRS) is what counts in terms of evolution, but investments in reproduction entail costs for an organism. The idea that telomere dynamics may be shaped in response to such costs is already established; however, we still lack information on whether this relation translates to overall fitness. Here, we quantified LRS (number of fledged young) and longitudinal telomere dynamics of small passerine birds—the blue tits ( Cyanistes caeruleus ). We found that individual telomere erosion rate was positively associated with lifetime fledgling number. Birds with more fledged young experienced increased telomere attrition. We show that telomere attrition rate, but not telomere length, is related to individual fitness and suggest that telomere dynamics may underlie reproductive costs experienced by animals as a consequence of prioritizing their lifetime fitness. This is the first study, to our knowledge, to provide evidence that more pronounced telomere erosion is associated with higher fitness gain.

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Section: Resultsmentioning

confidence: 99%

Birds with high lifetime reproductive success experience increased telomere loss

et al. 2019

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“…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.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2017

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BackgroundReproduction is an energetically expensive process that supposedly impairs somatic integrity in the long term, because resources are limited and have to be allocated between reproduction and somatic maintenance, as predicted by the life history trade-off model. The consequence of reduced investment in somatic maintenance is a gradual deterioration of function, i.e. senescence. However, this classical trade-off model gets challenged by an increasing number of contradicting studies. Here we report about an animal model, which adds more complexity to the ongoing debate. Ansell’s mole-rats are long-lived social subterranean rodents with only the founder pair reproducing, while most of their offspring remain in the parental burrow system and do not breed. Despite of a clear reproductive trade-off, breeders live up to twice as long as non-breeders, a unique feature amongst mammals.MethodsWe investigated mass-specific resting metabolic rates (msRMR) of breeders and non-breeders to gain information about the physiological basis underlying the reproduction-associated longevity in Ansell’s mole-rats. We assessed the thermoneutral zone (TNZ) for breeders and non-breeders separately by means of indirect calorimetry. We applied generalized linear mixed-effects models for repeated measurements using the msRMR in the respective TNZs.ResultsTNZ differed between reproductive and non-reproductive Ansell’s mole-rats. Contrary to classical aging models, the shorter-lived non-breeders had significantly lower msRMR within the thermoneutral zone compared to breeders.ConclusionThis is the first study reporting a positive correlation between msRMR and lifespan based on reproductive status. Our finding contradicts common aging theories, but supports recently introduced models which do not necessarily link reproductive trade-offs to lifespan reduction.

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“…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.…”

Section: Physical Activity Aging and "Effort"mentioning

confidence: 99%

Does Physical Activity Age Wild Animals?

Soulsbury

Halsey

2018

Front. Ecol. Evol.

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There is considerable interest in why the process of aging varies between individuals, both in humans and other animals. However, in animals, aging in terms of survival (demographic senescence) is understood in considerably more detail than in terms of declines in the body's functional capacity (functional senescence). Oxidative damage is probably an important component of the aging process in many species. Physical activity typically increases levels of oxidative stress, and many animals exhibit long and intense periods of active behavior. These observations raise a question that has not yet been addressed: while in humans, at least, activity is considered beneficial to health, could high intensity activity play a part in the rate that wild animals age? Studies to date suggest that increased "effort" can lead to reduced survival in free-living animals, but "effort" refers to different processes in different studies, and is rarely clarified or quantified. To understand the role of activity in functional senescence, studies must measure the detailed activity of free-ranging animals, possibly describing it in terms of intensity, frequency and duration, coupled with records of resultant physiological and DNA damage.

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Elevated reproduction does not affect telomere dynamics and oxidative stress

Cited by 17 publications

References 58 publications

Birds with high lifetime reproductive success experience increased telomere loss

Birds with high lifetime reproductive success experience increased telomere loss

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

Does Physical Activity Age Wild Animals?

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