Current versus future reproduction and longevity: a re-evaluation of predictions and mechanisms

Abstract

Oxidative damage is predicted to be a mediator of trade-offs between current reproduction and future reproduction or survival, but most studies fail to support such predictions. We suggest that two factors underlie the equivocal nature of these findings: (1) investigators typically assume a negative linear relationship between current reproduction and future reproduction or survival, even though this is not consistently shown by empirical studies; and (2) studies often fail to target mechanisms that could link interactions between sequential lifehistory events. Here, we review common patterns of reproduction, focusing on the relationships between reproductive performance, survival and parity in females. Observations in a range of species show that performance between sequential reproductive events can decline, remain consistent or increase. We describe likely bioenergetic consequences of reproduction that could underlie these changes in fitness, including mechanisms that could be responsible for negative effects being ephemeral, persistent or delayed. Finally, we make recommendations for designing future studies. We encourage investigators to carefully consider additional or alternative measures of bioenergetic function in studies of life-history trade-offs. Such measures include reactive oxygen species production, oxidative repair, mitochondrial biogenesis, cell proliferation, mitochondrial DNA mutation and replication error and, importantly, a measure of the respiratory function to determine whether measured differences in bioenergetic state are associated with a change in the energetic capacity of tissues that could feasibly affect future reproduction or lifespan. More careful consideration of the life-history context and bioenergetic variables will improve our understanding of the mechanisms that underlie the life-history patterns of animals.

Oxidative stress in aspic vipers facing pregnancy and water constraints

“…Furthermore, telomeres have been shown to shorten in response to both increased reproductive effort (Reichert et al, 2014) and stressful environmental conditions (Stier et al, 2014b(Stier et al, , 2015bMeillere et al, 2015;Simide et al, 2016). Additionally, recent work suggests that changes in mitochondrial bioenergetics and ROS production during reproduction are potential key mechanisms underlying the costs of reproduction (Zhang and Hood, 2016). Non-mammalian vertebrates like the aspic viper will offer great opportunities in the future to study such questions in a minimally invasive manner as their RBCs possess functional mitochondria, unlike those of mammalian species (Stier et al, 2013(Stier et al, , 2015a(Stier et al, , 2017.…”

“…However, the proximate physiological determinants of this cost remain under debate (Metcalfe and Monaghan, 2013;Zhang and Hood, 2016). Several studies have suggested oxidative stress as one potential physiological mediator of this life history trade-off (Monaghan et al, 2009;Stier et al, 2012;Metcalfe and Monaghan, 2013;Speakman et al, 2015).…”

Cellular metabolic rates and oxidative stress profiles in primary fibroblast cells isolated from virgin females, reproductively experienced females, and male Sprague-Dawley rats

“…Thus, reproduction in mammals is a period of high reproductive plasticity (Hood et al. ), with physiological changes that can alter a female's physiology for the remainder of her lifespan (Zhang and Hood ). We found that the primiparous and multiparous females showed no differences with respect to oxygen consumption and glycolytic rates compared with virgin females and had significantly lower rates of oxidative damage which was likely facilitated by the utilization of their endogenous antioxidant reserves.…”

“…Thus, we would expect that having offspring may negatively affect the metabolic and oxidative stress profiles of the mother, in terms of increased energy expenditure and potential increases in oxidative damage. However, pregnancy does not seem to negatively affect mitochondrial ATP production, and may even increase the number of antioxidants produced by the individual (Schmidt and Hood ; Zhang and Hood ). This indicates that a single pregnancy itself may not be inherently detrimental to mothers, and may even provide some physiologically protective effects.…”

Mitochondrial function and bioenergetic trade‐offs during lactation in the house mouse (Mus musculus)

“…Cells and organs may compensate for a drop in RCR by increasing the number of mitochondria present through mitochondrial biogenesis (Pichaud, Garratt, Ballard, & Brooks, 2013). In contrast, the P/O ratio targets the coupling efficiency of the mitochondria and substrate oxidation (Salin, Auer, Rey, Selman, & Metcalfe, 2015;Zhang & Hood, 2016). Change in P/O reflects changes in the proton motive force across the inner mitochondrial membrane due to a change in the activity of uncoupling proteins, adenine nucleotide transporters, and the fatty acid content of the lipid bilayer.…”