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

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.

On the modulation and maintenance of hibernation in captive dwarf lemurs.

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.

Food mobility and the evolution of grasping behaviour: a case study in strepsirrhine primates.

Manual grasping is widespread among tetrapods but is more prominent and dexterous in primates. Whether the selective pressures that drove the evolution of dexterous hand grasping involved the collection of fruit or predation on mobile insects remains an area of debate. One way to explore this question is to examine preferences for manual versus oral grasping of a moving object. Previous studies on strepsirrhines have shown a preference for oral grasping when grasping static food items and a preference for manual grasping when grasping mobile prey such as insects, but little is known about the factors at play. Using a controlled experiment with a simple and predictable motion of a food item, we tested and compared the grasping behaviours of 53 captive individuals belonging to 17 species of strepsirrhines while grasping swinging food items and static food items. The swinging motion increased the frequency of hand-use for all individuals. Our results provide evidence that the swinging motion of the food is a sufficient parameter to increase hand grasping in a wide variety of strepsirrhine primates. From an evolutionary perspective, this result gives some support to the idea that hand-grasping abilities evolved under selective pressure associated with the predation of food items in motion. Looking at a common grasping pattern across a large set of species, this study provides important insight into comparative approaches to understanding the evolution of the hand grasping of food in primates and potentially other tetrapod taxa.

Holding-on: co-evolution between infant carrying and grasping behaviour in strepsirrhines.

The origin and evolution of manual grasping remain poorly understood. The ability to cling requires important grasping abilities and is essential to survive in species where the young are carried in the fur. A previous study has suggested that this behaviour could be a pre-adaptation for the evolution of fine manipulative skills. In this study we tested the co-evolution between infant carrying in the fur and manual grasping abilities in the context of food manipulation. As strepsirrhines vary in the way infants are carried (mouth vs. fur), they are an excellent model to test this hypothesis. Data on food manipulation behaviour were collected for 21 species of strepsirrhines. Our results show that fur-carrying species exhibited significantly more frequent manual grasping of food items. This study clearly illustrates the potential novel insights that a behaviour (infant carrying) that has previously been largely ignored in the discussion of the evolution of primate manipulation can bring.