Many mammals use adaptive heterothermy (e.g., torpor, hibernation) to reduce metabolic demands of maintaining high body temperature ( T b ). Torpor is typically characterized by coordinated declines in T b and metabolic rate (MR) followed by active rewarming. Most hibernators experience periods of euthermy between bouts of torpor during which homeostatic processes are restored. In contrast, the common tenrec, a basoendothermic Afrotherian mammal, hibernates without interbout arousals and displays extreme flexibility in T b and MR. We investigated the molecular basis of this plasticity in tenrecs by profiling the liver proteome of animals that were active or torpid with high and more stable T b (∼32°C) or lower T b (∼14°C). We identified 768 tenrec liver proteins, of which 50.9% were differentially abundant between torpid and active animals. Protein abundance was significantly more variable in active cold and torpid compared with active warm animals, suggesting poor control of proteostasis. Our data suggest that torpor in tenrecs may lead to mismatches in protein pools due to poor coordination of anabolic and catabolic processes. We propose that the evolution of endothermy leading to a more realized homeothermy of boreoeutherians likely led to greater coordination of homeostatic processes and reduced mismatches in thermal sensitivities of metabolic pathways.
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Hibernation slows epigenetic ageing in yellow-bellied marmots
Species that hibernate generally live longer than would be expected based solely on their body size. Hibernation is characterized by long periods of metabolic suppression (torpor) interspersed by short periods of increased metabolism (arousal). The torpor–arousal cycles occur multiple times during hibernation, and it has been suggested that processes controlling the transition between torpor and arousal states cause ageing suppression. Metabolic rate is also a known correlate of longevity; we thus proposed the ‘hibernation–ageing hypothesis’ whereby ageing is suspended during hibernation. We tested this hypothesis in a well-studied population of yellow-bellied marmots (
- NSF-PAR ID:
- 10365144
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Ecology & Evolution
- Volume:
- 6
- Issue:
- 4
- ISSN:
- 2397-334X
- Page Range / eLocation ID:
- p. 418-426
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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During hibernation, animals cycle between torpor and arousal. These cycles involve dramatic but poorly understood mechanisms of dynamic physiological regulation at the level of gene expression. Each cycle, Brown Adipose Tissue (BAT) drives periodic arousal from torpor by generating essential heat. We applied digital transcriptome analysis to precisely timed samples to identify molecular pathways that underlie the intense activity cycles of hibernator BAT. A cohort of transcripts increased during torpor, paradoxical because transcription effectively ceases at these low temperatures. We show that this increase occurs not by elevated transcription but rather by enhanced stabilization associated with maintenance and/or extension of long poly(A) tails. Mathematical modeling further supports a temperature-sensitive mechanism to protect a subset of transcripts from ongoing bulk degradation instead of increased transcription. This subset was enriched in a C-rich motif and genes required for BAT activation, suggesting a model and mechanism to prioritize translation of key proteins for thermogenesis.
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Abstract Under life‐history theories of ageing, increased senescence should follow relatively high reproductive effort. This expectation has rarely been tested against senescence varying between and within the two sexes, although such an approach may clarify the origins of sex‐specific ageing in the context of a given mating system.
Nazca boobies (
Sula granti ; a seabird) practise serial monogamy and biparental care. A male‐biased population sex ratio results in earlier and more frequent breeding by females. Based on sex‐specific reproductive schedules, females were expected to show faster age‐related decline for survival and reproduction. Within each sex, high reproductive effort in early life was expected to reduce late‐life performance and accelerate senescence.Longitudinal data were used to (a) evaluate the sex specificity of reproductive and actuarial senescence and then (b) test for early‐/late‐life fitness trade‐offs within each sex. Within‐sex analyses inform an interpretation of sex differences in senescence based on costs of reproduction. Analyses incorporated individual heterogeneity in breeding performance and cohort‐level differences in early‐adult environments.
Females showed marginally more intense actuarial senescence and stronger age‐related declines for fledging success. The opposite pattern (earlier and faster male senescence) was found for breeding probability. Individual reproductive effort in early life positively predicted late‐life reproductive performance in both sexes and thus did not support a causal link between early‐reproduction/late‐life fitness trade‐offs and sex differences in ageing. A high‐quality diet in early adulthood reduced late‐life survival (females) and accelerated senescence for fledging success (males).
This study documents clear variation in ageing patterns—by sex, early‐adult environment and early‐adult reproductive effort—with implications for the role mating systems and early‐life environments play in determining ageing patterns. Absent evidence for a disposable soma mechanism, patterns of sex differences in senescence may result from age‐ and condition‐dependent mate choice interacting with this population's male‐biased sex ratio and mate rotation.
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Key points Vascular oxidative stress increases with advancing age.
We hypothesized that resistance vessels develop resilience to oxidative stress to protect functional integrity and tested this hypothesis by exposing isolated pressurized superior epigastric arteries (SEAs) of old and young mice to H2O2.
H2O2‐induced death was greater in smooth muscle cells (SMCs) than endothelial cells (ECs) and lower in SEAs from old
vs . young mice; the rise in vessel wall [Ca2+]iinduced by H2O2was attenuated with ageing, as was the decline in noradrenergic vasoconstriction; genetic deletion of IL‐10 mimicked the effects of advanced age on cell survival.Inhibiting NO synthase or scavenging peroxynitrite reduced SMC death; endothelial denudation or inhibiting gap junctions increased SMC death; delocalization of cytochrome C activated caspases 9 and 3 to induce apoptosis.
Vascular cells develop resilience to H2O2during ageing by preventing Ca2+overload and endothelial integrity promotes SMC survival.
Abstract Advanced age is associated with elevated oxidative stress and can protect the endothelium from cell death induced by H2O2. Whether such protection occurs for intact vessels or differs between smooth muscle cell (SMC) and endothelial cell (EC) layers is unknown. We tested the hypothesis that ageing protects SMCs and ECs during acute exposure to H2O2(200 µ
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