Abstract

ABSTRACTMetabolism 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 used indirect calorimetry to characterize metabolic phenotypes of the desert-adapted cactus mouse (Peromyscus eremicus) in response to variable environmental conditions that mimic their native environment versus those recorded under constant warm and constant cool conditions, with 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 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 contributes 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.

Highlights

  • Our planet is undergoing unprecedented environmental change, which is exerting new, strong selective pressures on species, forcing them to relocate, adapt in situ or risk extinction

  • Circadian rhythms are observed in most mammals and are in part governed by genetics and the interplay between the perception of environmental change and neuroendocrine-mediated physiological responses (MirandaAnaya et al, 2019)

  • Comparing metabolic responses between sexes and across constant and variable environments, we show that (i) males are more prone to dehydration than females, (ii) patterns of metabolic variation are well tuned to environmental cycling, and (iii) lipogenesis offers a potential mechanism of endogenous water production, employed only under variable environmental conditions

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Summary

Introduction

Our planet is undergoing unprecedented environmental change, which is exerting new, strong selective pressures on species, forcing them to relocate, adapt in situ or risk extinction. Of equal importance are the physiological adaptations of desert species, which are predicted to play an important role in species’ responses to climate change (Kearney et al, 2009; Boyles et al, 2011; Huey et al, 2012). Examination of the physiological responses of organisms to both stable and dynamic environmental conditions provides a window into the flexibility of such responses to changing environments and will be increasingly important for understanding and predicting species’ responses to climate change (Garland and Carter, 1994; Dalziel et al, 2009; Easterling et al, 2000; IPCC, 2012, 2018; Huey et al, 2012)

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