Sex- and trait-specific silver-spoon effects of developmental environments, on ageing

Abstract

The environment organisms experience during development can have effects which carry over into their adult lives. These environments not only affect adult traits at a given point in time, but also how these traits change with age. Generally, favorable developmental environments lead to more optimal adult traits while stressful environments are deleterious ("silver-spoon effect"). But whether developmental environments affect how whole-organism performance traits change with age or whether they affect males and females differently lacks evidence. Here, we test whether experiencing favorable developmental environments leads to "silver-spoon effects" on life-history traits and whole-organism flight performance of males and females by manipulating developmental density in Callosobruchus maculatus. We further test whether such effects are mediated by an individual's reproductive status by comparing traits of mated versus virgin females. We show that although developmental crowding has no effect on flight performance of either sex, on male adult lifespan, or on female age-dependent survival, it is detrimental to female lifespan and fecundity, as well as female age-dependent reproduction, suggesting that females are more sensitive to differences in developmental density. Additionally, we show that flight traits change with age and differ not only between males and females, which is reflective of sex-specific lifehistories and behavior, but also between virgin and mated females. Our study is important for understanding sex-specific responses to developmental environments in life-history, behavioral, and ecologically important traits which may affect resource allocation, dispersal, and mating strategies, hence fitness.

Sex‐specific aging in animals: Perspective and future directions

“…A sex‐specific environmental effect on lifespan has been explicitly demonstrated, for example, in the seed beetle Callosobruchus maculatus (Sanghvi et al, 2021 ). Sanghvi and colleagues manipulated larval density to determine the impact of early life environment quality on flight performance, fecundity, and lifespan.…”

“…Sanghvi and colleagues manipulated larval density to determine the impact of early life environment quality on flight performance, fecundity, and lifespan. They found that female fecundity and lifespan are negatively affected by poor larval environment, while male fecundity and lifespan are not affected (Sanghvi et al, 2021 ). Another example is a study of Seychelles warbler, Acrocephalus sechellensis , which demonstrates that the presence of non‐breeding or co‐breeding helper females increased survival for older dominant females significantly, but did not do so for dominant males.…”

Effects of developmental and adult environments on ageing

“…2010), possibly by selecting for sex‐specific pace of life syndromes (Immonen et al, 2018). For example, in seed beetles, males and females respond differently to the presence and density of competitors during the larval stage, leading to sex‐specific differences in a variety of life‐history traits (Iglesias‐Carrasco et al 2020; Sanghvi et al, 2021).…”

“…Senescence occurs as a consequence of relaxed selection on fitness‐related traits in older individuals due to trade‐offs between life‐history components (Rose and Charlesworth, 1980; Stearns, 1989). However, the rate at which individuals age may depend on a range of factors such as their sex and external environment (e.g., Sanghvi et al, 2021). Although there is some support for favorable developmental conditions leading to slower reproductive and survival senescence (Hayward, Wilson et al, 2013, Cooper and Kruuk, 2018, Sanghvi et al, 2021), an alternative hypothesis suggests that individuals experiencing good environments may senesce faster due to increased investment in growth and reproduction when young (Adler et al, 2016; Hooper et al 2017; Hunt et al, 2004; Spagopoulou et al., 2020).…”

“…However, the rate at which individuals age may depend on a range of factors such as their sex and external environment (e.g., Sanghvi et al, 2021). Although there is some support for favorable developmental conditions leading to slower reproductive and survival senescence (Hayward, Wilson et al, 2013, Cooper and Kruuk, 2018, Sanghvi et al, 2021), an alternative hypothesis suggests that individuals experiencing good environments may senesce faster due to increased investment in growth and reproduction when young (Adler et al, 2016; Hooper et al 2017; Hunt et al, 2004; Spagopoulou et al., 2020). Additionally, senescence can also depend on the interactions between developmental and adult environments, as seen in studies that test for compensatory growth.…”