Life History Trade-offs within the Context of Mitochondrial Hormesis

Abstract

Evolutionary biologists have been interested in the negative interactions among life history traits for nearly a century, but the mechanisms that would create this negative interaction remain poorly understood. One variable that has emerged as a likely link between reproductive effort and longevity is oxidative stress. Specifically, it has been proposed that reproduction generates free radicals that cause oxidative stress and, in turn, oxidative stress damages cellular components and accelerates senescence. We propose that there is limited support for the hypothesis because reactive oxygen species (ROS), the free radicals implicated in oxidative damage, are not consistently harmful. With this review, we define the hormetic response of mitochondria to ROS, termed mitochondrial hormesis, and describe how to test for a mitohormetic response. We interpret existing data using our model and propose that experimental manipulations will further improve our knowledge of this response. Finally, we postulate how the mitohormetic response curve applies to variation in animal performance and longevity.

Fig. 1

The predicted response to ROS exposure under a linear response and mitohormetic response. The response to ROS can be indicated by its impact on mitochondrial performance or on an animal’s fitness. Under a linear response (black line), ROS becomes increasing damaging with relative exposure. Under a mitohormetic response, modest levels of ROS benefits performance while high levels negatively impact metabolism and fitness (adapted from Zhang and Hood 2016).

Fig. 2

Litter size at birth (A) and cumulative mass of the litter at weaning (B) for females with and without access to a running wheel before reproduction. Adapted from Zhang et al (2018a).

Fig. 3

Change in the mitochondrial ROS production (A, B), lipid peroxidation (4HNE) (C, D), and complex 1 activity (E, F) in the liver (A, C, E) and skeletal muscle (B, D, F) of virgin wild-derived mice exposed to 500 rad x-radiation. Note that if data had only been collected 1 day post-exposure (black bars) or 10 days post-exposure (white bars), the interpretation of the response would have been very different. Different letters above the bars indicate statistical significance. Adapted from Zhang et al (2018b).

Fig. 4

Effect of interacting stressors on change in ROS levels on cellular performance and fitness. Figure include examples of (A) positive and negative additive effects, synergistic effects (B), antagonistic effects (C), and priming effects (D).

Fig. 5

Common pattern of energy allocated to each reproductive event across the life of a female. Total energy allocated to reproduction is typically indicated by offspring number or mass but many also be indicated by direct measure of the energy content of young.