Abstract

As with many physiological performance traits, the capacity of endotherms to thermoregulate declines with age. Aging compromises both the capacity to conserve or dissipate heat and the thermogenesis, which is fueled by aerobic metabolism. The rate of metabolism, however, not only determines thermogenic capacity but can also affect the process of aging. Therefore, we hypothesized that selection for an increased aerobic exercise metabolism, which has presumably been a crucial factor in the evolution of endothermic physiology in the mammalian and avian lineages, affects not only the thermoregulatory traits but also the age-related changes of these traits. Here, we test this hypothesis on bank voles (Myodes glareolus) from an experimental evolution model system: four lines selected for high swim-induced aerobic metabolism (A lines), which have also increased the basal, average daily, and maximum cold-induced metabolic rates, and four unselected control (C) lines. We measured the resting metabolic rate (RMR), evaporative water loss (EWL), and body temperature in 72 young adult (4 months) and 65 old (22 months) voles at seven ambient temperatures (13–32°C). The RMR was 6% higher in the A than in the C lines, but, regardless of the selection group or temperature, it did not change with age. However, EWL was 12% higher in the old voles. An increased EWL/RMR ratio implies either a compromised efficiency of oxygen extraction in the lungs or increased skin permeability. This effect was more profound in the A lines, which may indicate their increased vulnerability to aging. Body temperature did not differ between the selection and age groups below 32°C, but at 32°C it was markedly higher in the old A-line voles than in those from other groups. As expected, the thermogenic capacity, measured as the maximum cold-induced oxygen consumption, was decreased by about 13% in the old voles from both selection groups, but the performance of old A-line voles was the same as that of the young C-line ones. Thus, the selection for high aerobic exercise metabolism attenuated the adverse effects of aging on cold tolerance, but this advantage has been traded off by a compromised coping with hot conditions by aged voles.

Highlights

  • Aging is one of the most challenging issues in medicine and biomedical research (Wahlich et al, 2019) and is a puzzling phenomenon within evolutionary–ecology

  • The network of biochemical processes associated with aerobic metabolism is recognized as an important factor behind aging at the cellular level, and, since the seminal work of Denham Harman (1956), the hypothesis linking a high rate of metabolism with accelerated aging has been subject to a vivid and continuing debate (Holloszy and Smith, 1986; Speakman et al, 2004; Andziak et al, 2006; Brys et al, 2007; Gems and Doonan, 2009; Salmon et al, 2010; Rudolf et al, 2017; Viña, 2019)

  • The resting metabolic rate (RMR) increased with increasing activity index (p < 0.05), and the RMR estimated for the modal value of standard deviation (SD) = 0.02 was 3–5% higher in comparison to that estimated for SD = 0.05 at all Ta values below 32◦C

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Summary

Introduction

Aging is one of the most challenging issues in medicine and biomedical research (Wahlich et al, 2019) and is a puzzling phenomenon within evolutionary–ecology (review in Flouris and Piantoni, 2015). Despite innumerous studies on the relation between pairs of the three features – the rates of metabolism, thermoregulation, and aging – the question has apparently not yet been addressed. We tackle this question using a unique model of experimental evolution, lines of a common non-laboratory rodent, the bank vole, Myodes glareolus, selected for the high rate of aerobic exercise metabolism (Sadowska et al, 2008; Rudolf et al, 2017; Stawski et al, 2017)

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