Lifetime fitness consequences of early‐life ecological hardship in a wild mammal population

Abstract

Early‐life ecological conditions have major effects on survival and reproduction. Numerous studies in wild systems show fitness benefits of good quality early‐life ecological conditions (“silver‐spoon” effects). Recently, however, some studies have reported that poor‐quality early‐life ecological conditions are associated with later‐life fitness advantages and that the effect of early‐life conditions can be sex‐specific. Furthermore, few studies have investigated the effect of the variability of early‐life ecological conditions on later‐life fitness. Here, we test how the mean and variability of early‐life ecological conditions affect the longevity and reproduction of males and females using 14 years of data on wild banded mongooses (Mungos mungo). Males that experienced highly variable ecological conditions during development lived longer and had greater lifetime fitness, while those that experienced poor early‐life conditions lived longer but at a cost of reduced fertility. In females, there were no such effects. Our study suggests that exposure to more variable environments in early life can result in lifetime fitness benefits, whereas differences in the mean early‐life conditions experienced mediate a life‐history trade‐off between survival and reproduction. It also demonstrates how early‐life ecological conditions can produce different selection pressures on males and females.

Spontaneous abortion as a response to reproductive conflict in the banded mongoose

“…Rainfall in the study site correlates with invertebrate abundance (e.g. [14]), so cumulative rainfall for 60 days before the birth of the communal litter was used as a proxy for resource abundance during gestation. In the banded mongoose, pups born in communal litters compete for helpers postnatally, and the breeding success of dominant females declines with increasing female group size [15].…”

Does Physical Activity Age Wild Animals?

“…Similar detail at the physiological level is missing in wild animals (Reichard, 2016), but we know that some phenotypic, physiological, and behavioral traits can age asynchronously (Elliott et al, 2014;Hayward et al, 2015;Kervinen et al, 2015), in a way similar to in ourselves. At the same time, we have a comparatively detailed picture of the interconnected nature of aging between humans and the environment (Dato et al, 2017), and while similar evidence is accruing in wild animals (Nussey et al, 2008;Marshall et al, 2015), our understanding is far from complete (Hammers et al, 2015).…”

Silver‐spoon upbringing improves early‐life fitness but promotes reproductive ageing in a wild bird

“…While a large body of evidence supports these theoretical predictions on the population level, very little is known about the individual variation in ageing rates. There is a general agreement in the field that early‐life environmental conditions can shape the life‐history of an adult organism and explain much of the individual variation in ageing rates (Monaghan 2008; Marshall et al 2017; Cooper & Kruuk 2018), but there is little consensus regarding the direction of the effect. Good environmental conditions during development can result in lifelong positive effects on physiology, reproduction and longevity (Lindström 1999; van de Pol et al 2006a; Nussey et al 2007; Hayward et al 2013; Cooper & Kruuk 2018) (‘silver‐spoon’ hypothesis – Grafen 1990).…”

“…Good environmental conditions during development can result in lifelong positive effects on physiology, reproduction and longevity (Lindström 1999; van de Pol et al 2006a; Nussey et al 2007; Hayward et al 2013; Cooper & Kruuk 2018) (‘silver‐spoon’ hypothesis – Grafen 1990). Alternatively, organisms raised in good natal environments can invest heavily in growth and early‐life reproduction, resulting in accelerated senescence in late‐life (Hunt et al 2004; Bonduriansky & Brassil 2005; Hooper et al 2017; Marshall et al 2017) (‘live‐fast die‐young’ hypothesis – Promislow & Harvey 1990). These studies suggest that organisms can allocate resources to reproduction and somatic maintenance depending on their early‐life environmental conditions, and that high latent costs of increased early‐life growth and reproduction, under favourable conditions, can result in accelerated ageing (Adler et al 2016; Hooper et al 2017).…”