Disentangling environmental drivers of circadian metabolism in desert-adapted mice

Abstract

Metabolism is a complex phenotype shaped by natural environmental rhythms, as well as behavioral, morphological, and physiological adaptations. Metabolism has been historically studied under constant environmental conditions, but new methods of continuous metabolic phenotyping now offer a window into organismal responses to dynamic environments, and enable identification of abiotic controls and the timing of physiological responses relative to environmental change. We use indirect calorimetry to characterize metabolic phenotypes of the desert-adapted cactus mouse (Peromyscus eremicus) in response variable environmental conditions that mimic their native environment versus those recorded under constant warm and constant cool conditions, while using a constant photoperiod and full access to resources. We found significant sexual dimorphism, with males being more prone to dehydration than females. Under circadian environmental variation, most metabolic shifts occurred prior to physical environmental change and the timing was disrupted under both constant temperature-humidity treatments. The ratio of CO2 produced to O2 consumed (the respiratory quotient) reached greater than 1.0, only during the light phase under diurnally variable conditions, a pattern that strongly suggests that lipogenesis is contributing to the production of energy and endogenous water. Our results are consistent with historical descriptions of circadian torpor in this species (torpid by day, active by night), but reject the hypothesis that torpor is initiated by food restriction or negative water balance.

High total water loss driven by low-fat diet in desert-adapted mice

“…RQ values exceed 1.0 when anabolism of fat exceeds catabolism (i.e., DNL) (Abreu-Vieira et al, 2015;Benedict, 1937;Levin et al, 2017) or during aerobic exercise (Whipp, 2007;Zagatto et al, 2012). In the experiment described here and in previous experiments on P. eremicus (Colella et al, 2021b), RQ is only greater than 1.0 during the light phase when animals are inactive, supporting DNL. While carbohydrates, fats, or protein are all burned as fuel, if present in excess, adipose fat can be easily stored in animals (Barboza et al, 2009).…”

“…Like other desert mammals, P. eremicus rely on evaporative cooling for thermoregulation and thus, is expected to employ a frugal water economy when water intake is limited. We demonstrate diet-specific differences in the rate of evaporative water loss (RWL) and serum electrolyte values, and a consistent pattern of daily de novo lipogenesis (DNL, Colella et al, 2021b) that is not limited by dietary composition. These results support the hypothesis that water conservation is at least partially tied to diet composition and provide a deeper understanding of how desert animals maintain water homeostasis in hot, arid environments.…”

“…Mice were randomly assigned to one of two feeding groups: A standard diet group (SD - LabDiet® 5015*, 26.101% fat, 19.752% protein, 54.148% carbohydrates, food quotient [FQ] 0.89, supplemental file 3) or a low-fat diet group (LFD - Modified LabDiet® 5015 [5G0Z], 6.6% fat, 22.8% protein, 70.6% carbohydrates, FQ = 0.92, supplemental file 4). Animals were housed individually in 9.5L animal chambers inside a larger, walk-in environmental chamber built to replicate temperature, humidity, and photoperiodic conditions of the Sonoran Desert (Colella et al, 2021c; Kordonowy et al, 2017). Each animal chamber contained dried cellulose-based bedding, and animals were provided food and water ad libitum .…”

“…Metabolic phenotyping data were collected using a previously described (Colella et al, 2021b) commercially available respirometry system purchased from Sable Systems International. Physiological data were collected following the methods outlined in Whitfield et al (2015) and Colella et al (2021b). Oxygen consumption (VO 2 ml min -1 ), carbon dioxide production (VCO 2 ml min -1 ), and water vapor (WVP, kPa) were continually measured during 72 hr trials.…”

“…Given the relationship between dietary composition and metabolic water production, the current study examines the effects of dietary fat content on the metabolic physiology of the desert-adapted cactus mouse. To accomplish this, we extend previously characterized circadian metabolic patterns for males and females (Colella et al, 2021b) to rates of metabolism and water loss in animals fed an experimental diet low in fat, but otherwise unchanged. Thereby testing the role that dietary fat has on water balance, which has a direct connection to fitness.…”