Are trade‐offs really the key drivers of ageing and life span?

Abstract

1. Current thinking in life-history theory and the biology of ageing suggests that ageing rates, and consequently life spans, evolve largely as a function of trade-offs with reproduction. While various evolutionary constraints are generally acknowledged to exist, their potential role in determining ageing rates is rarely considered.2. This review integrates three types of information to assess the relative importance of constraints and trade-offs in shaping ageing rates: (a) empirical work on the presence of intraspecific trade-offs; (b) theoretical work on factors limiting the force of trade-offs; and (c) consideration of the biological mechanisms of ageing, as currently understood. 3. At the empirical level, evidence for intraspecific trade-offs is mixed, including some surprising failures to observe a trade-off in model organisms. At the theoretical level, the presence of multiple currencies and nonlinearity can weaken the strength and/or generality of trade-offs. Additionally, trade-offs among lowerlevel functions, such as between sources of mortality, can create constraints at higher organizational levels, for example such that reductions in reproduction are unable to produce decreases in ageing rate. In terms of ageing mechanisms, some mechanisms, such as the regulation of IGF-1 and related pathways, seem to agree quite well with trade-offs as a driving force; however, other mechanisms, such as dysregulation of the vertebrate stress response and stem cell exhaustion, seem more likely to impose constraints than to mediate trade-offs. 4. Taken together, these findings suggest that trade-offs alone are insufficient to understand how ageing rates evolve; instead, both trade-offs and constraints likely play important roles in shaping evolutionary patterns, with their relative importance varying across taxa. Accordingly, it is time to revisit the broad assumption that survival-reproduction trade-offs are the key force structuring much of lifehistory variation and the evolution of ageing rates. K E Y W O R D S ageing, constraint, cost of reproduction, disposable soma, life history, physiology, senescence, trade-off 154 | Functional Ecology COHEN Et al. | 155Functional Ecology COHEN Et al. | 157Functional Ecology COHEN Et al.

Life History Transitions at the Origins of Agriculture: A Model for Understanding How Niche Construction Impacts Human Growth, Demography and Health

“…For example, early studies suggested that producing offspring is correlated with reduced lifespan among parents of both sexes (28,29), though in general the strongest evidence is for mothers. However, several studies have failed to demonstrate negative associations between reproduction and lifespan (123,124), and the evidence that greater reproductive effort promotes faster ageing through oxidative damage is inconsistent (26). We suggest that a wider range of metabolic traits relative to fitness merit consideration.…”

“…Moreover, other studies of the Tsimané found that despite their high fertility rates, markers of cardio-metabolic disease are amongst the lowest reported in human populations (127,128). The costs of reproduction may therefore be both "condition dependent, " i.e., varying in association with broader ecological conditions, and also outcome-dependent, i.e., varying across different markers of maintenance (26). In addition, they may also be shaped by experience in early life.…”

“…Early work on life history theory considered that there were three competing functions (maintenance, growth, and reproduction) giving rise to three potential binary trade-offs (14,22), as illustrated In Figure 1A. Particular attention was directed to the trade-off between reproduction and survival, whereby producing more offspring was assumed to reduce investment in homeostatic maintenance (e.g., through mechanisms such as oxidative stress), thereby accelerating ageing and shortening parental lifespan (26). For example, experimental studies in animals tested the effect of imposing a greater reproductive burden (e.g., augmenting brood size in birds) on parental lifespan (27), while observational analyses in humans tested for inverse correlations between fertility and lifespan (28,29).…”

A negative association between horn length and survival in a weakly dimorphic ungulate

“…Such positive co‐covariations can arise when the relative variation in resource acquisition exceeds the relative variation in resource allocation among individuals (van Noordwijk & de Jong, ). In addition, trade‐offs may only be evident under poor environmental conditions (Cohen et al, ). In large herbivores, poor environmental conditions can originate from multiple and often inter‐related factors such as high density, harsh weather, and low food availability.…”

“…However, recent studies in the weakly dimorphic Alpine chamois (Rupicapra rupicapra) showed nonsignificant trends toward decreased longevity with increasing horn growth in males and females (Bleu, Loison, & Toïgo, 2014;Corlatti, Storch, Filli, & Anderwald, 2017). Such relationships may be stronger in populations experiencing poor environmental conditions, as reported for survival costs of reproduction (Cohen, Coste, Li, Bourg, & Pavard, 2019).…”