Ageing with a silver-spoon: A meta-analysis of the effect of developmental environment on senescence

Abstract

What determines variation between individuals in how they senesce, and are environmental conditions experienced during development relevant to late‐life performance? We report a meta‐analysis of studies of wild populations to determine how the quality of the environment experienced during development affects rates of survival and reproductive senescence. From studies of 14 bird or mammal species, we calculated effect sizes for the interaction between the effects of environmental quality during development and age in predicting survival (N = 18) or reproduction (N = 30) over time in late life. We found no evidence that developmental environment affected rates of survival senescence (βmean = –1.2 × 10−4 ± 0.022SE). However, a better developmental environment was associated with slower rates of reproductive senescence in late life (βmean = 0.062 ± 0.023SE), indicating a small, but significant, “silver‐spoon” effect of early‐life conditions that persisted through to late life. Our results illustrate how the effects of environmental conditions during development can persist throughout life, and indicate one possible cause of phenotypic plasticity in senescence.

Individual variation in early‐life telomere length and survival in a wild mammal

“…Pioneering laboratory studies using controlled environments have provided important insights into senescence patterns, but cannot explain the remarkable variation in the onset and rate of senescence in wild populations, where selection acts under naturally varying conditions (Partridge & Gems, ). Hence, studies of wild populations have informed understanding of how early‐life environments shape individual senescence patterns (Cooper & Kruuk, ; Lemaitre et al, ; Nussey, Froy, Lemaitre, Gaillard, & Austad, ). This understanding has been further improved by quantification of extrinsic effects through biomarkers that reflect ecological effects that are otherwise difficult to measure (Bebbington et al, ; Spurgin et al, ).…”

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).…”

“…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). 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).…”

Development time mediates the effect of larval diet on ageing and mating success of male antler flies in the wild

“…Other studies have reported similarly complex phenotypic effects of early life environmental quality: rich larval diets can lead to increased reproductive effort and a shortened lifespan [17,20,21], although we observed the opposite effect here. Given the complex influence of early-life conditions reported in this and other studies, it is not surprising that two recent meta-analyses failed to detect consistent silver spoon effects on lifespan or actuarial senescence in laboratory or wild populations [30,31].…”

“…Thus, the ultimate effect of early-life environmental quality on senescence is unclear. Two recent meta-analyses failed to detect consistent silver-spoon effects across taxa on longevity or actuarial senescence, and only a small effect on reproductive senescence [30,31]. Nevertheless, some studies have reported significant increases in lifespan and reduced senescence for individuals that experienced high quality developmental environments [6,9,32].…”