What can seasonal models teach us about energy balance?

Abstract

Torpid states are used by many endotherms to save energy during winter. During torpor, metabolic rate is downregulated to fractions of resting metabolic rate and often associated with a severe drop in body temperature that challenges mammalian physiology. Understanding the mechanisms regulating this extreme depression of metabolism bears enormous potential for biomedical research. Torpor behavior has been extensively studied in the Djungarian hamster, also known as Siberian hamster. It is dependent on many preparatory adaptations of physiological and endocrine systems that are likely to be integrated by the hypothalamus eventually controlling metabolism. Although substantial knowledge exists about prerequisites and characteristics of torpor in this species, the cascade of events and their mechanisms of action are not well understood. This review summarizes the current state of knowledge about mechanisms of metabolic regulation in the Djungarian hamster focusing on the potential roles of thyroid hormone and glucose metabolism.

Body Temperature and Activity Adaptation of Short Photoperiod-Exposed Djungarian Hamsters (Phodopus sungorus): Timing, Traits, and Torpor

“…The high variability in adaptation is considered to be natural and not indicative of the negative effects of domestication and genetic bottlenecks ( Figala et al, 1973 ), as a hamster population should benefit from a certain degree of individual flexibility and variation to cope with acute and unpredictable changes in environmental conditions ( Ruf et al, 1991 , 1993 ). Nevertheless, since the Siberian winter is usually long and harsh, nature should have selected for hamsters with a fast and strong adaptation in response to the decreasing photoperiod length, followed by flexible torpor use as anticipation of acute energetic challenges, which are not given in laboratory conditions ( Diedrich et al, 2015 , 2020 ).…”

“…In approach 2, "never torpor" hamsters appeared to respond more weakly in all the observed parameters, suggesting a different metabolic programming of hamsters never expressing torpor at given circumstances (Cubuk et al, 2016;Diedrich et al, 2020). The most promising indicators of "never torpor" hamsters might be a higher body temperature during scotophase over the entire course of SP adaptation (Figure 6C) and a smaller delta body temperature and, therefore, variation during both scoto-and photophases (Figure 7).…”

“…Approximately 3 months later, the morphological and physiological adaptations are largely completed, and the animals start to express spontaneous daily torpor. They use this metabolic downstate to save additional energy during their resting phase (photophase), while they are normothermic and active during the scotophase ( Heldmaier and Steinlechner, 1981b ; Diedrich et al, 2020 ). This complex temporal organization requires sensitivity to photoperiod length, based on daily light information as zeitgeber .…”

What is the physiological role of hypothalamic tanycytes in metabolism?

“…These models allow us to modulate tanycyte functions and measure the physiological consequences for energy balance (16,17). Seasonal animals also constitute a powerful model to study tanycyte functions (18,19). Indeed, these animals, including hamsters, sheep, F344 rats, and birds, naturally integrate the light/dark cycle throughout the year to adapt their physiology to ensure optimal longterm control of energy and, subsequently, to maximize reproduction.…”

Adipose Tissue Immunometabolism and Apoptotic Cell Clearance

“…VDR is also necessary for development of breast WAT [ 88 ]. Vitamin D biosynthesis is sunlight-dependent and seasonal light cycle changes are known to determine metabolic rate oscillations [ 89 ]. Indeed, a correlation exists between adult body mass index and season of birth, and some studies have reported an increased rate of obesity among winter-born individuals [ 90 , 91 ].…”