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 life-history 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.

Keywords: Cost of reproduction; Life-history traits; Longevity; Mitochondrial function; Oxidative stress; Reactive oxygen species.

Fig. 1.

Common patterns of reproductive performance versus parity. (A) As current and future reproduction are often though to trade off, this panel represents the hypothetical relationship that would be expected if trade-offs were to occur at each reproductive event. (B–D) Each of the species listed display a pattern of reproduction that is observed in numerous species (additional references given in text). (B) An increase and later plateau in reproductive performance is observed in the northern elephant seal (Le Boeuf and Reiter, 1988). (C) An increase, plateau and late-life decline in reproductive performance is observed in the Eurasian sparrowhawk (Newton et al., 1981). (D) An increase in reproductive performance with parity is common among species with indeterminate growth such as the black rockfish (Bobko and Berkeley, 2004). In these examples, the relationship between current and future reproduction changes with parity, dashed line ‘a’ indicates negative interactions, dashed line ‘b’ indicates neutral interactions, and dashed line ‘c’ indicates positive interactions between current and future reproduction.

Fig. 2.

Common patterns of maternal parity versus risk of death. (A) This panel represents the hypothetical relationship that would be expected if females experienced increased risk of death with each reproductive event. All other panels represent the most common relationships between female parity and risk of death observed among vertebrate species. (B) Exponential decay curve is found for 58% of the species that have been investigated. (C) A left-skewed U-curve is found for 24% of the investigated species. (D) A right-skewed U-curve is found for 12% of the species that have been investigated. In many of these examples, the relationship between parity and risk of death changes over time: dashed line ‘a’ indicates negative interactions, dashed line ‘b’ indicates neutral interactions and dashed line ‘c’ indicates positive interactions between parity and risk of death. Modified from Proaktor et al. (2007).

Fig. 3.

The relationships between reactive oxygen species production and relative mitochondrial respiratory function under a linear response and mitochondrial hormesis. Traditional predictions suggest a linear negative relationship between increasing amounts of ROS and mitochondrial respiratory function (indicated by the red line). The concept of mitohormesis (blue curve) indicates a non-linear dose–response relationship, where low doses of ROS exposure increase mitochondrial repiratory fucntion, whereas higher doses decrease mitochondrial repiratory function. Figure modified from Ristow and Schmeisser (2014), incorporating the findings of Schulz et al. (2007), Schmeisser et al. (2013).