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

Abstract

Availability of essential food resources is one of the most important drivers of survival and to persist in environments where critical resource abundance is changing, animals must either relocate or adapt in place. Testing an animal’s ability to respond to alternative conditions can reveal differences in physiological responses. We used flow-through respirometry to characterize metabolic phenotypes of the desert-adapted cactus mouse (Peromyscus eremicus) under diurnally variable environmental conditions that mimic the Sonoran Desert and treated mice with two different diets; a standard diet and a low-fat diet. We found significant diet-specific differences in the rate of water loss and serum electrolyte values. Mice fed the low-fat diet lost more water relative to those eating the standard diet and patterns of de novo lipogenesis are not limited by dietary composition. Our results are consistent with the hypothesis that diet contributes to water homeostasis. Compared to other desert animals, rodents have limited capacity to dissipate heat using evaporative cooling, limiting thermoregulatory performance at higher temperatures. We predict that a mismatch in physiological requirements and environmental conditions could significantly impact small mammal survival in desert environments if optimal foods become less abundant, as may be the case given climate change.

Impacts of dietary fat on multi tissue gene expression in the desert-adapted cactus mouse

“…Key electrolytes sensitive to hydration status, such as serum Na, osmolality, and Hct, are elevated in animals fed the LF diet indicating a difference in water balance. However, synthetic markers of pathological renal impairment, BUN, and Cr, did not significantly differ between treatments (further discussed in Blumstein et al, 2024). In the study described here, we found several significant genes identified in our consensus gene sets related to the management of Na ( SLC9A5 [lung], TNR [hypothalamus], SLC38A4 and SLC17A1 [kidney], Supplemental Table 2) and osmolality ( ADCYAP1R1 and PKLR [hypothalamus], ITLN1 [lung], SLC2A9 [liver], GJB1 and PPP1R3G [kidney], Supplemental Table 2), suggesting that varied fat content results in a solute concentration response.…”

“…Additionally, PDK1 and PDHA1 , convergent genes in cellular energy metabolism (described above) are both significantly differentially expressed in the GI, with PDHA1 being upregulated in mice fed the LF diet and PDK1 upregulated in mice fed the SD. Further, 202 genes were significantly downregulated in the LF treatment in the GI and were grouped into the GO term cellular response to insulin stimulus [GO:0032869], as well as nine genes from the consensus GI list ( ADCY2, ATP1A2, HKDC1, KCNMA1, PPP1R3B, PRKCB, RIMS2, RYR2, SNAP25, Supplemental Table 2) and three genes from the consensus liver list (HNF4A, IGFALS, ITIH2, Supplemental Table 2) related to insulin were downregulated suggesting that the mitochondria are successfully contributing to overall metabolic homeostasis, further explaining the insignificant differences in EE reported in Blumstein et al (2024).…”

“…As the planet continues to undergo unprecedented climate change, increased desertification and a decrease in free water availability is predicted (IPCC, 2019; Mirzabaev et al, 2019). Several studies have demonstrated or predicted distributional changes in extant species in response to changing climate (Moritz et al, 2008; Parmesan, 2006), but fewer have examined the physiological (Bijlsma and Loeschcke, 2005; Blumstein and MacManes, 2023; Blumstein et al, 2024; Gabriel, 2005; Ramirez et al, 2022) and genomic (Blumstein and MacManes, 2024; Cheviron et al, 2014; Colella et al, 2021; MacManes, 2017; Tigano et al, 2020) mechanisms that may allow animals to adapt in place.…”

“…Faced with the natural variation in resource availability, opportunistic animals have the capacity to significantly impact their internal water balance and in turn, their survival. When comparing a standard diet to a low fat diet, Blumstein et al (2024) described elevated rates of water loss during the warmer, drier light phase compared to the dark phase and variations in serum electrolyte levels suggestive of dehydration for cactus mice fed a low fat diet, suggesting dietary fat is significant in regulating water balance during long-term physiological experiments. Even minor variation in water balance can profoundly affect cognitive function (Riebl and Davy, 2013), physical performance, and ultimately, survival and reproductive success (Cunningham et al, 2021).…”

When the tap runs dry: The multi-tissue gene expression and physiological responses of water deprivedPeromyscus eremicus

“…Captive born, sexually mature, non-reproductive healthy male and female P. eremicus were reared in an environmental chamber designed to simulate the Sonoran desert (Blumstein et al, 2022; Blumstein and MacManes, 2023; Colella et al, 2021; Kordonowy et al, 2017). All mice were subjected to standard animal care procedures before the experiment which included a health assessment conducted by licensed veterinary staff following animal care procedures guidelines established by the American Society of Mammologists (Sikes et al, 2016) and approved by the University of New Hampshire Institutional Animal Care and Use Committee under protocol number 210602.…”