Limits to sustained energy intake. XXXIV. Can the heat dissipation limit (HDL) theory explain reproductive aging?

According to the heat dissipation limit (HDL) theory, reproductive performance is limited by the capacity to dissipate excess heat. We tested the novel hypotheses that (1) the age-related decline in reproductive performance is due to an age-related decrease of heat dissipation capacity and (2) the limiting mechanism is more severe in animals with high metabolic rates. We used bank voles (Myodes glareolus) from lines selected for high swim-induced aerobic metabolic rate, which have also increased basal metabolic rate, and unselected control lines. Adult females from three age classes - young (4 months), middle-aged (9 months) and old (16 months) - were maintained at room temperature (20°C), and half of the lactating females were shaved to increase heat dissipation capacity. Old females from both selection lines had a decreased litter size, mass and growth rate. The peak-lactation average daily metabolic rate was higher in shaved than in unshaved mothers, and this difference was more profound among old than young and middle-aged voles (P=0.02). In females with large litters, milk production tended to be higher in shaved (least squares mean, LSM±s.e.: 73.0±4.74 kJ day-1) than in unshaved voles (61.8±4.78 kJ day-1; P=0.05), but there was no significan"t effect of fur removal on the growth rate [4.47±2.29 g (4 days-1); P=0.45]. The results provide mixed support of the HDL theory and no support for the hypotheses linking the differences in reproductive aging with either a deterioration in thermoregulatory capability or genetically based differences in metabolic rate.

Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection Experiment.

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.

Rest-Phase Hypothermia Reveals a Link Between Aging and Oxidative Stress: A Novel Hypothesis.

In endotherms, growth, reproduction, and survival are highly depended on energy metabolism. Maintenance of constant body temperature can be challenging for endotherms under continuously changing environmental conditions, such as low or high ambient temperatures or limited food. Thus, many birds may drop body temperature below normothermic values during the night, known as rest-phase hypothermia, presumably to decrease energy metabolism. Under the assumption of the positive link between aerobic metabolism and reactive oxygen species, it is reasonable to suggest that low body temperature, a proxy of energy metabolism, will affect oxidative stress of the birds. Aging may considerably affect behavior, performance and physiology in birds and still requires further investigation to understand age-specific changes along the lifespan of the organism. Until today, age-specific rest-phase hypothermic responses and their effect on oxidant-antioxidant status have never been investigated. We exposed 25 zebra finches (Taeniopygia guttata) of three age classes, 12 young birds (1.1-1.3 years old), 8 middle-aged (2.4-2.8 years old), and 5 old birds (4.2-7.5 years old) to day-long food deprivation or provided them normal access to food under thermoneutral conditions. We compared night-time body temperature, measured through implanted data loggers, and quantified plasma oxidative status (uric acid, antioxidant capacity, and d-ROM assay) the following morning. We found age-related differences in night-time body temperature following a day-long food deprivation while all three age groups remained normothermic in the night following a day with access to food. The lowest minimum body temperature (LSM ± SE: 36.6 ± 0.2°C) was observed in old individuals during rest-phase hypothermia. Surprisingly, these old birds also revealed the highest levels of plasma oxidative damage, while young and middle-aged birds maintained higher night-time body temperature and showed lower values of oxidative damage. These results lead us to propose a novel hypothesis on how aging may lead to an accumulation of oxidative damage; the impaired physiological capacity to thermoregulate with advancing age does increase the risk of oxidative stress under challenging conditions. When energy is limited, the risk to encounter oxidative stress is increasing via a compensation to defend normothermic body temperatures.