Telomere attrition and restoration in the normal teleost Oryzias latipes are linked to growth rate and telomerase activity at each life stage

Hatakeyama, Hitoshi; Yamazaki, Hiromi; Nakamura, Kenichi; Izumiyama-Shimomura, Naotaka; Aida, Junko; Suzuki, Hiroyoshi; Tsuchida, Shuichi; Matsuura, M.; Takubo, Kaiyo; Ishikawa, Naoshi

doi:10.18632/aging.100873

Cited by 39 publications

(47 citation statements)

References 68 publications

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“…To our knowledge, late-growth elongation, like we observed, is only known for one species, the fish Oryzias latipes [54]. Increased telomerase activity is the proposed mechanism for developmental telomere elongation observed in O. latipes [54], so this is likely the same mechanism contributing to our results. Although we did not measure telomerase directly, we measured an increase in telomere length from shortest length on day 15 back to hatch day length by day 30, similar to what was shown in O. latipes .…”

Section: Discussionsupporting

confidence: 67%

Telomeres shorten and then lengthen before fledging in Magellanic penguins (Spheniscus magellanicus)

Cerchiara

Risques

Prunkard

et al. 2017

Aging

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For all species, finite metabolic resources must be allocated toward three competing systems: maintenance, reproduction, and growth. Telomeres, the nucleoprotein tips of chromosomes, which shorten with age in most species, are correlated with increased survival. Chick growth is energetically costly and is associated with telomere shortening in most species. To assess the change in telomeres in penguin chicks, we quantified change in telomere length of wild known-age Magellanic penguin (Spheniscus magellanicus) chicks every 15 days during the species’ growth period, from hatching to 60 days-of-age. Magellanic penguins continue to grow after fledging so we also sampled a set of 1-year-old juvenile penguins, and adults aged 5 years. Telomeres were significantly shorter on day 15 than on hatch day but returned to their initial length by 30 days old and remained at that length through 60 days of age. The length of telomeres of newly hatched chicks, chicks aged 30, 45 and 60 days, juveniles, and adults aged 5 years were similar. Chicks that fledged and those that died had similar telomere lengths. We show that while telomeres shorten during growth, Magellanic penguins elongate telomeres to their length at hatch, which may increase adult life span and reproductive opportunities.

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Section: Discussionsupporting

confidence: 67%

Telomeres shorten and then lengthen before fledging in Magellanic penguins (Spheniscus magellanicus)

Cerchiara

Risques

Prunkard

et al. 2017

Aging

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“…Previous studies have shown that heat stress reduced telomere length in the Siberian sturgeon Acipenser baerii (Simide, Angelier, Gaillard, & Stier, 2016) and the brown trout Salmo trutta (Debes et al, 2016). Fishes show life stage-specific telomere lengths because they exhibit lifelong somatic growth and express telomerase across tissues and throughout all life stages (Anchelin, Murcia, Alcaraz-Pérez, García-Navarro, & Cayuela, 2011;Hartmann et al, 2009;Hatakeyama et al, 2016). Fishes show life stage-specific telomere lengths because they exhibit lifelong somatic growth and express telomerase across tissues and throughout all life stages (Anchelin, Murcia, Alcaraz-Pérez, García-Navarro, & Cayuela, 2011;Hartmann et al, 2009;Hatakeyama et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Carry‐over effects of early thermal conditions on somatic and germline oxidative damages are mediated by compensatory growth in sticklebacks

Kim

Noguera

Velando

2018

Journal of Animal Ecology

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Most studies of climate change impacts focus on the effects of summer temperatures, which can immediately impact fitness of breeders, but winter temperatures are expected to have a greater impact on development and growth of animals with long‐lasting consequences. Exposure to warmer temperatures can increase cellular oxidative damage in ectotherms. Yet, it is unknown whether thermal stress during early life has prolonged effects on oxidative status during adulthood. In an experiment using F1 fish originated from a wild three‐spined stickleback population at the southern edge of its European distribution, we examined whether experimental thermal conditions experienced in winter had carry‐over effects on oxidative status and telomere length, a marker of accumulated stress, in the soma and germline during adulthood. For this, oxidative DNA damage, enzymatic antioxidant activities and telomere length were measured three months after the termination of the temperature manipulation. In addition, we tested whether such delayed effects, if any, were due to individuals’ compensatory growth after experiencing unfavourable growth conditions in winter. Warm acclimation during winter induced increased levels of oxidative DNA damage in muscle and sperm and increased enzymatic antioxidant defences in muscle during the breeding season. Telomere length of adult fish was not influenced by thermal conditions experienced during early life. Winter temperature manipulation influenced fish to alter the temporal pattern of growth trajectories across the juvenile and adult stages. Fish reared in warm winter conditions grew at a slower rate than the controls during the period of temperature manipulation then accelerated body mass gain to catch up during the breeding season. Faster somatic growth during the breeding season incurred a higher cost in terms of oxidative damage in the warm‐treated individuals. For the first time, we experimentally show the long‐lasting detrimental effects of thermal stress on and the positive link between catch‐up growth and oxidative DNA damage in the soma and germline. Winter temperature increases due to climate change can reduce fertility and survival of fish by inducing catch‐up growth. The detrimental effects of winter climate change may accumulate across generations through the pre‐mutagenic DNA damage in the germline.

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“…by up‐regulation of oxidative defence mechanisms; von Zglinicki et al ., ), or restore telomeres (e.g. by increasing telomerase activity; Hatakeyama et al ., ), would be an active process, and thus by definition require energy and be involved in trade‐offs with other energy‐demanding processes, like growth.…”

Section: Discussionmentioning

confidence: 99%

Telomere attrition and growth: a life‐history framework and case study in common terns

Vedder

Verhulst

Bauch

et al. 2017

J of Evolutionary Biology

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The relationship between growth and age-specific telomere length, as a proxy of somatic state, is increasingly investigated, but observed patterns vary and a predictive framework is lacking. We outline expectations based on the assumption that telomere maintenance is costly and argue that individual heterogeneity in resource acquisition is predicted to lead to positive covariance between growth and telomere length. However, canalization of resource allocation to the trait with a larger effect on fitness, rendering that trait relatively invariant, can cause the absence of covariance. In a case study of common tern (Sterna hirundo) chicks, in which hatching order is the main determinant of variation in resource acquisition within broods, we find that body mass, but not telomere length or attrition, varies with hatching order. Moreover, body mass and growth positively predict survival to fledging, whereas telomere length and attrition do not. Using a novel statistical method to quantify standardized variance in plasticity, we estimate between-individual variation in telomere attrition to be only 12% of that of growth. Consistent with the relative invariance of telomere attrition, we find no correlation between age-specific body mass or growth and telomere attrition. We suggest that common tern chicks prioritize investment in long-term somatic state (as indicated by canalization of telomere maintenance) over immediate survival benefits of growth as part of an efficient brood reduction strategy that benefits the parents. As such, interspecific variation in the growth-telomere length relationship may be explained by the extent to which parents benefit from rapid mortality of excess offspring.

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Telomere attrition and restoration in the normal teleost Oryzias latipes are linked to growth rate and telomerase activity at each life stage

Cited by 39 publications

References 68 publications

Telomeres shorten and then lengthen before fledging in Magellanic penguins (Spheniscus magellanicus)

Telomeres shorten and then lengthen before fledging in Magellanic penguins (Spheniscus magellanicus)

Carry‐over effects of early thermal conditions on somatic and germline oxidative damages are mediated by compensatory growth in sticklebacks

Telomere attrition and growth: a life‐history framework and case study in common terns

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