Early-life reproduction is associated with increased mortality risk but enhanced lifetime fitness in pre-industrial humans

Abstract

The physiology of reproductive senescence in women is well understood, but the drivers of variation in senescence rates are less so. Evolutionary theory predicts that early-life investment in reproduction should be favoured by selection at the cost of reduced survival and faster reproductive senescence. We tested this hypothesis using data collected from preindustrial Finnish church records. Reproductive success increased up to age 25 and was relatively stable until a decline from age 41. Women with higher early-life fecundity (ELF; producing more children before age 25) subsequently had higher mortality risk, but high ELF was not associated with accelerated senescence in annual breeding success. However, women with higher ELF experienced faster senescence in offspring survival. Despite these apparent costs, ELF was under positive selection: individuals with higher ELF had higher lifetime reproductive success. These results are consistent with previous observations in both humans and wild vertebrates that more births and earlier onset of reproduction are associated with reduced survival, and with evolutionary theory predicting trade-offs between early reproduction and later-life survival. The results are particularly significant given recent increases in maternal ages in many societies and the potential consequences for offspring health and fitness.

Effects of macronutrient intake on the lifespan and fecundity of the marula fruit fly, Ceratitis cosyra (Tephritidae): Extreme lifespan in a host specialist

“…Trade‐offs between reproduction and lifespan are common: in general, investing in reproduction is costly and usually shortens lifespan (Flatt, 2011) and accordingly reproductive effort in short‐lived species is typically intense and early in life. Conversely, long‐lived species usually exhibit weak early reproductive effort (Hayward, Nenko, & Lummaa, 2015; Kirkwood & Rose, 1991). However, the GF shows us that particular nutrients can mediate trade‐offs and the severity of trade‐offs can differ between the sexes.…”

General conclusion to the special issue Moving forward on individual heterogeneity

“…Thus, the most appropriate distribution for their annual fecundity (sensu Allainé et al 1987) is a Poisson or generalized Poisson regression (Kendall and Wittmann 2010). Conversely, long-lived mammals, like elephants, whales, or humans, usually produce only a single offspring per reproductive attempt, with long inter-birth intervals (Kraus et al 2001, Hayward et al 2015, Lee et al 2016). In such cases, annual fecundity is usually modelled with a logistic regression.…”

Elevated reproduction does not affect telomere dynamics and oxidative stress

“…The cost of reproduction is often detected in experimental studies in terms of diminished body condition and survival (Nur 1984a; Daan et al 1996; Flatt 2011; Hayward et al 2015), subsequent fecundity of parents and offspring and offspring survival (Gustafsson and Sutherland 1988; Deerenberg et al 1996) and as such constitutes an important support for life-history theory. It is generally assumed that life-history trade-offs have to be driven by various physiological mechanisms; however, those mechanisms still remain equivocal.…”

“…Eroding telomeres are strongly involved in cellular and organismal ageing (Monaghan and Haussmann 2006) and seem to predict life expectancy (Bize et al 2009) whereas accumulating oxidative damage alone may lead to accelerated ageing (Sohal and Weindruch 1996). Since reproductive activity is positively associated with the ageing phenotype, elucidating actuarial, survival-related senescence (Nur 1984a; Flatt 2011; Hayward et al 2015), the idea arises that telomeres and oxidative stress may serve as biomarkers of reproduction-associated decreases in survival probability. Reproduction elevates metabolic rate (Deerenberg et al 1995; Skibiel et al 2013) due to higher workload (Nur 1984b; Tinbergen and Verhulst 2000), which potentially leads to overproduction of telomere-damaging ROS (Alonso-Alvarez et al 2004; Wiersma et al 2004).…”