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Abstract
Heterothermy allows organisms to cope with fluctuating environmental conditions. The use of regulated hypometabolism allows seasonal heterothermic species to cope with annual resource shortages and thus to maximize survival during the unfavorable season. This comes with deep physiological remodeling at each seasonal transition to allow the organism to adjust to the changing environment. In the wild, this adaptation is highly beneficial and largely overcomes potential costs. However, researchers recently proposed that it might also generate both ecological and physiological costs for the organism. Here, we propose new perspectives to be considered when analyzing adaptation to seasonality, in particular considering these costs. We propose a list of putative costs, including DNA damage, inflammatory response to fat load, brain and cognitive defects, digestive malfunction and immunodeficiency, that should receive more attention in future research on physiological seasonality. These costs may only be marginal at each transition event but accumulate over time and therefore emerge with age. In this context, studies in captivity, where we have access to aging individuals with limited extrinsic mortality (e.g., predation), could be highly valuable to experimentally assess the costs of physiological flexibility. Finally, we offer new perspectives, which should be included in demographic models, on how the adaptive value of physiological flexibility could be altered in the future in the context of global warming.
Highlights
In seasonal environments, resource availability fluctuates over the year, mainly between a phase of resource abundance and a phase of resource shortage
SH use seasonal changes in the photoperiod as an environmental cue to synchronize their physiology to the environment and to adjust their metabolic rate to undergo either hibernation or daily torpor during unfavorable phases (Geiser, 2017)
To better emphasize the originality of these results, we provided in Figures 2E,F two alternative models that should fit the data if senescence of physiological transitions leads to an increase in the magnitude of mortality fluctuations without (Figure 2E) or with (Figure 2F) a positive AFT effect on the aging rate
Summary
Resource availability fluctuates over the year, mainly between a phase of resource abundance and a phase of resource shortage. We expect physiological costs of seasonal heterothermy to emerge from imperfect biological regulations, imperfect seasonal regulation of competing functions and from suboptimal phenotypic matching with environmental changes This recurrent phenotypic remodeling contributes to the accumulation of damage and to the aging process in SH (see Figure 1A). Major focus has been placed on the potential of telomerase reactivation in anti-aging strategies, there exists little evidence that telomerase activity is impaired with age and that this translates into altered repair capacity (Anchelin et al, 2011) Another potential physiological cost of heterothermy is the risk associated with massive variations in body condition and, more fat reserves (Figure 1). Depending on its severity, infection will lead to either resistance (through microbicidal mechanisms, for example) or tolerance (through management of collateral damage; Medzhitov et al, 2012; Ganeshan et al, 2019; Steiner and Romanovsky, 2019)
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