Metabolic and genomic adaptations to winter fattening in a primate species, the grey mouse lemur (Microcebus murinus)

Terrien, Jérémy; Gaudubois, M; Champeval, Delphine; Zaninotto, Vincent; Roger, L.; Riou, Jean‐François; Aujard, Fabienne

doi:10.1038/ijo.2017.195

Cited by 22 publications

(69 citation statements)

References 48 publications

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“…Thus, exposure to contrasting environmental conditions, leading to the expression of seasonal phenotypes may, in fact, help maintain a healthy dwarf lemur population in captivity, if hibernation is expressed in moderation 54 . A “renaturalized” captive dwarf lemur population will set the stage for future investigations of the mechanisms underlying hibernation expression and its regulation, for example exploring protective mechanisms that allow dwarf lemurs to tolerate spikes in sugar or lipid metabolism without showing signs of illness 20 .…”

Section: Discussionmentioning

confidence: 99%

On the modulation and maintenance of hibernation in captive dwarf lemurs

Blanco

Greene

Schopler

et al. 2021

Sci Rep

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In nature, photoperiod signals environmental seasonality and is a strong selective “zeitgeber” that synchronizes biological rhythms. For animals facing seasonal environmental challenges and energetic bottlenecks, daily torpor and hibernation are two metabolic strategies that can save energy. In the wild, the dwarf lemurs of Madagascar are obligate hibernators, hibernating between 3 and 7 months a year. In captivity, however, dwarf lemurs generally express torpor for periods far shorter than the hibernation season in Madagascar. We investigated whether fat-tailed dwarf lemurs (Cheirogaleus medius) housed at the Duke Lemur Center (DLC) could hibernate, by subjecting 8 individuals to husbandry conditions more in accord with those in Madagascar, including alternating photoperiods, low ambient temperatures, and food restriction. All dwarf lemurs displayed daily and multiday torpor bouts, including bouts lasting ~ 11 days. Ambient temperature was the greatest predictor of torpor bout duration, and food ingestion and night length also played a role. Unlike their wild counterparts, who rarely leave their hibernacula and do not feed during hibernation, DLC dwarf lemurs sporadically moved and ate. While demonstrating that captive dwarf lemurs are physiologically capable of hibernation, we argue that facilitating their hibernation serves both husbandry and research goals: first, it enables lemurs to express the biphasic phenotypes (fattening and fat depletion) that are characteristic of their wild conspecifics; second, by “renaturalizing” dwarf lemurs in captivity, they will emerge a better model for understanding both metabolic extremes in primates generally and metabolic disorders in humans specifically.

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Section: Discussionmentioning

confidence: 99%

On the modulation and maintenance of hibernation in captive dwarf lemurs

Blanco

Greene

Schopler

et al. 2021

Sci Rep

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“…All individuals from this population were monitored from birth to death and provided with ad libitum water and shelter availability. Food was delivered in quantities that were sufficiently high to maximize reproduction and survival, while not too abundant to prevent excessive fattening and the negative consequences of long‐term obesity (Terrien et al, ). We hypothesize that under such conditions, with nonlimiting resources and virtually no extrinsic mortality, reproducing would not negatively affect future survival.…”

Section: Introductionmentioning

confidence: 99%

Female reproduction bears no survival cost in captivity for gray mouse lemurs

Landes

Henry

Hardy

et al. 2019

Ecology and Evolution

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The survival cost of reproduction has been revealed in many free‐ranging vertebrates. However, recent studies on captive populations failed to detect this cost. Theoretically, this lack of survival/reproduction trade‐off is expected when resources are not limiting, but these studies may have failed to detect the cost, as they may not have fully accounted for potential confounding effects, in particular interindividual heterogeneity. Here, we investigated the effects of current and past reproductive effort on later survival in captive females of a small primate, the gray mouse lemur. Survival analyses showed no cost of reproduction in females; and the pattern was even in the opposite direction: the higher the reproductive effort, the higher the chances of survival until the next reproductive event. These conclusions hold even while accounting for interindividual heterogeneity. In agreement with aforementioned studies on captive vertebrates, these results remind us that reproduction is expected to be traded against body maintenance and the survival prospect only when resources are so limiting that they induce an allocation trade‐off. Thus, the cost of reproduction has a major extrinsic component driven by environmental conditions.

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“…However, arousal from a hypometabolic state may generate a brief but massive peak in oxidative damage (Figure 1). In mouse lemurs, when metabolic activity increases, DNA oxidative damage increases and relative telomere length decreases (Terrien et al, 2017). Telomere shortening during this seasonal transition may be an adaptive response.…”

Section: Oxidative Stress and Genomic Instabilitymentioning

confidence: 99%

“…Recent work on the mouse lemur has shown that the relative expression of phospho-IRS-1 was enhanced in muscle during torpor but decreased in white adipose tissue, thus suggesting an inhibition of insulin/IGF-1 signaling during torpor in these tissues (Tessier et al, 2015). In parallel, animals seem to be protected from an inflammatory response during massive fattening (Terrien et al, 2017). Further work is needed to determine to what extent the mechanisms that prevent insulin resistance and inflammation during fattening are altered with age.…”

Section: Excess Fat and The Associated Inflammatory Responsementioning

confidence: 99%

“…This will help us to better understand physiological processes such as circannual biological rhythms and reproductive cycles (Cayetanot et al, 2005). In addition, such studies may shed light on the mechanisms associated with degrading health conditions at old ages (high survival syndrome of hibernators; Turbill et al, 2011) and better prevent physiological disorders such as obesity (Terrien et al, 2017).…”

Section: Conclusion and Perspectives In The Context Of Global Warmingmentioning

confidence: 99%

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Flexibility Is Costly: Hidden Physiological Damage From Seasonal Phenotypic Transitions in Heterothermic Species

et al. 2020

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Heterothermy allows organisms to cope with fluctuating environmental conditions. The use of regulated hypometabolism allows seasonal heterothermic species to cope with annual resource shortages and thus to maximize survival during the unfavorable season. This comes with deep physiological remodeling at each seasonal transition to allow the organism to adjust to the changing environment. In the wild, this adaptation is highly beneficial and largely overcomes potential costs. However, researchers recently proposed that it might also generate both ecological and physiological costs for the organism. Here, we propose new perspectives to be considered when analyzing adaptation to seasonality, in particular considering these costs. We propose a list of putative costs, including DNA damage, inflammatory response to fat load, brain and cognitive defects, digestive malfunction and immunodeficiency, that should receive more attention in future research on physiological seasonality. These costs may only be marginal at each transition event but accumulate over time and therefore emerge with age. In this context, studies in captivity, where we have access to aging individuals with limited extrinsic mortality (e.g., predation), could be highly valuable to experimentally assess the costs of physiological flexibility. Finally, we offer new perspectives, which should be included in demographic models, on how the adaptive value of physiological flexibility could be altered in the future in the context of global warming.

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Metabolic and genomic adaptations to winter fattening in a primate species, the grey mouse lemur (Microcebus murinus)

Abstract: Altogether, these results show that mouse lemurs undergo deep physiological and genomic seasonal changes, without ever reaching a pathological stage. Further investigation is needed to decipher the underlying mechanisms, which may well be highly relevant for human therapeutic strategies.

Cited by 22 publications

References 48 publications

On the modulation and maintenance of hibernation in captive dwarf lemurs

On the modulation and maintenance of hibernation in captive dwarf lemurs

Female reproduction bears no survival cost in captivity for gray mouse lemurs

Flexibility Is Costly: Hidden Physiological Damage From Seasonal Phenotypic Transitions in Heterothermic Species

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