Of fruits and fats: high-sugar diets restore fatty acid profiles in the white adipose tissue of captive dwarf lemurs

Blanco, Marina B.; Greene, Lydia K.; Ellsaesser, L N; Schopler, Bobby; Davison, Mark A.; Ostrowski, C; Klopfer, Peter H.; Fietz, Joanna; Ehmke, Erin

doi:10.1098/rspb.2022.0598

Cited by 8 publications

(5 citation statements)

References 46 publications

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“…Certain polyunsaturated fatty acids (PUFAs) and saturated fatty acids were significantly enriched in hibernating S. raddei. Fatty acids in general, and PUFAs in particular, are the principal fuel sources for hibernating animals as they have a low melting point and are readily metabolized even at low temperatures (Blanco et al 2022). PUFAs may also protect mammalian hearts in cold environments.…”

Section: Discussionmentioning

confidence: 99%

The intestinal microbiota and metabolic profiles of Strauchbufo raddei underwent adaptive changes during hibernation

et al. 2023

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The intestinal microbiota help regulate hibernation in vertebrates. However, it needs to be established how hibernation modulates the gut microbiome and intestinal metabolism. In the present study, we used an artificial hibernation model to examine the responses of the gut microbiota of the Strauchbufo raddei to the environmental changes associated with this behavior. Hibernation significantly lowered the diversity of the microbiota and altered the microbial community of the gut. Proteobacteria, Firmicutes, and Bacteroidota were the major bacterial phyla in the intestines of S. raddei. However, Firmicutes and Proteobacteria predominated in the gut of active and hibernating S. raddei, respectively. Certain bacterial genera such as Pseudomonas, Vibrio, Ralstonia, and Rhodococcus could serve as biomarkers distinguishing hibernating and non‐hibernating S. raddei. The gut microbiota was more resistant to environmental stress in hibernating than active S. raddei. Moreover, metabolomics revealed that metabolites implicated in fatty acid biosynthesis were highly upregulated in the intestines of hibernating S. raddei. The metabolites that were enriched during hibernation enabled S. raddei to adapt to the low temperatures and the lack of exogenous food that are characteristic of hibernation. A correlation analysis of the intestinal microbiota and their metabolites revealed that the gut microbiota might participate in the metabolic regulation of hibernating S. raddei. The present study clarified the modifications that occur in the intestinal bacteria and their symbiotic relationship with their host during hibernation. These findings are indicative of the adaptive changes in the metabolism of amphibians under different environmental conditions.

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Section: Discussionmentioning

confidence: 99%

The intestinal microbiota and metabolic profiles of Strauchbufo raddei underwent adaptive changes during hibernation

et al. 2023

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“…During the fattening and active seasons, dwarf lemurs are maintained under stable warm conditions (22°C–25°C). During the fattening season, they are fed a high-sugar diet (∼15 g fresh fruit, ∼3 g monkey biscuit, 2 g dried fruit), whereas during the active season they are fed a high-fat diet (∼12 g fruit and veggie mix, 6 g monkey biscuit, 2 mealworms) ( Blanco et al, 2022b ). This regimen mimics the natural foraging patterns of wild populations ( Fietz and Ganzhorn, 1999 ) and helps mediate seasonal fat deposition and depletion ( Blanco et al, 2022b ).…”

Section: Methodsmentioning

confidence: 99%

“…During the lean season, six of our subjects remained under stable warm conditions and were fed a calorie-reduced, high-fat diet ( Blanco et al, 2022b ). The remaining subjects were transferred to hibernacula rooms.…”

Section: Methodsmentioning

confidence: 99%

Seasonal variation in glucose and insulin is modulated by food and temperature conditions in a hibernating primate

Blanco,

Greene,

Ellsaesser

et al. 2023

Front. Physiol.

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Feast-fast cycles allow animals to live in seasonal environments by promoting fat storage when food is plentiful and lipolysis when food is scarce. Fat-storing hibernators have mastered this cycle over a circannual schedule, by undergoing extreme fattening to stockpile fuel for the ensuing hibernation season. Insulin is intrinsic to carbohydrate and lipid metabolism and is central to regulating feast-fast cycles in mammalian hibernators. Here, we examine glucose and insulin dynamics across the feast-fast cycle in fat-tailed dwarf lemurs, the only obligate hibernator among primates. Unlike cold-adapted hibernators, dwarf lemurs inhabit tropical forests in Madagascar and hibernate under various temperature conditions. Using the captive colony at the Duke Lemur Center, we determined fasting glucose and insulin, and glucose tolerance, in dwarf lemurs across seasons. During the lean season, we maintained dwarf lemurs under stable warm, stable cold, or fluctuating ambient temperatures that variably included food provisioning or deprivation. Overall, we find that dwarf lemurs can show signatures of reversible, lean-season insulin resistance. During the fattening season prior to hibernation, dwarf lemurs had low glucose, insulin, and HOMA-IR despite consuming high-sugar diets. In the active season after hibernation, glucose, insulin, HOMA-IR, and glucose tolerance all increased, highlighting the metabolic processes at play during periods of weight gain versus weight loss. During the lean season, glucose remained low, but insulin and HOMA-IR increased, particularly in animals kept under warm conditions with daily food. Moreover, these lemurs had the greatest glucose intolerance in our study and had average HOMA-IR values consistent with insulin resistance (5.49), while those without food under cold (1.95) or fluctuating (1.17) temperatures did not. Remarkably low insulin in dwarf lemurs under fluctuating temperatures raises new questions about lipid metabolism when animals can passively warm and cool rather than undergo sporadic arousals. Our results underscore that seasonal changes in insulin and glucose tolerance are likely hallmarks of hibernating mammals. Because dwarf lemurs can hibernate under a range of conditions in captivity, they are an emerging model for primate metabolic flexibility with implications for human health.

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“…When researchers mimic hibernation‐promoting conditions (e.g. by providing high‐sugar fruits for fattening or food restriction, cold temperatures, or altered photoperiods), captive lemurs show patterns of fat deposition, torpor, and lipid metabolism that more closely resemble those of in‐situ hibernating conspecifics (Blanco et al ., 2022). It may seem counterintuitive that food restriction could be beneficial; yet it is a key component of successful hibernation, without which naturally hibernating animals may experience physiological and metabolic dysfunction in captivity.…”

Section: Microbiome Variation Between In‐situ and Ex‐situ Conspecificsmentioning

confidence: 99%

Integrating microbiome science and evolutionary medicine into animal health and conservation

Bornbusch,

Power,

Schulkin

et al. 2023

Biological Reviews

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Microbiome science has provided groundbreaking insights into human and animal health. Similarly, evolutionary medicine – the incorporation of eco‐evolutionary concepts into primarily human medical theory and practice – is increasingly recognised for its novel perspectives on modern diseases. Studies of host–microbe relationships have been expanded beyond humans to include a wide range of animal taxa, adding new facets to our understanding of animal ecology, evolution, behaviour, and health. In this review, we propose that a broader application of evolutionary medicine, combined with microbiome science, can provide valuable and innovative perspectives on animal care and conservation. First, we draw on classic ecological principles, such as alternative stable states, to propose an eco‐evolutionary framework for understanding variation in animal microbiomes and their role in animal health and wellbeing. With a focus on mammalian gut microbiomes, we apply this framework to populations of animals under human care, with particular relevance to the many animal species that suffer diseases linked to gut microbial dysfunction (e.g. gut distress and infection, autoimmune disorders, obesity). We discuss diet and microbial landscapes (i.e. the microbes in the animal's external environment), as two factors that are (i) proposed to represent evolutionary mismatches for captive animals, (ii) linked to gut microbiome structure and function, and (iii) potentially best understood from an evolutionary medicine perspective. Keeping within our evolutionary framework, we highlight the potential benefits – and pitfalls – of modern microbial therapies, such as pre‐ and probiotics, faecal microbiota transplants, and microbial rewilding. We discuss the limited, yet growing, empirical evidence for the use of microbial therapies to modulate animal gut microbiomes beneficially. Interspersed throughout, we propose 12 actionable steps, grounded in evolutionary medicine, that can be applied to practical animal care and management. We encourage that these actionable steps be paired with integration of eco‐evolutionary perspectives into our definitions of appropriate animal care standards. The evolutionary perspectives proposed herein may be best appreciated when applied to the broad diversity of species under human care, rather than when solely focused on humans. We urge animal care professionals, veterinarians, nutritionists, scientists, and others to collaborate on these efforts, allowing for simultaneous care of animal patients and the generation of valuable empirical data.

show abstract

Of fruits and fats: high-sugar diets restore fatty acid profiles in the white adipose tissue of captive dwarf lemurs

Cited by 8 publications

References 46 publications

The intestinal microbiota and metabolic profiles of Strauchbufo raddei underwent adaptive changes during hibernation

The intestinal microbiota and metabolic profiles of Strauchbufo raddei underwent adaptive changes during hibernation

Seasonal variation in glucose and insulin is modulated by food and temperature conditions in a hibernating primate

Integrating microbiome science and evolutionary medicine into animal health and conservation

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