A benign juvenile environment reduces the strength of antagonistic pleiotropy and genetic variation in the rate of senescence

Abstract

Summary The environment can play an important role in the evolution of senescence because the optimal allocation between somatic maintenance and reproduction depends on external factors influencing life expectancy.The aims of this study were to experimentally test whether environmental conditions during early life can shape senescence schedules, and if so, to examine whether variation among individuals or genotypes with respect to the degree of ageing differs across environments.We tested life‐history plasticity and quantified genetic effects on the pattern of senescence across different environments within a reaction norm framework by using an experiment on the three‐spined stickleback (Gasterosteus aculeatus, Linnaeus) in which F1 families originating from a wild annual population experienced different temperature regimes.Male sticklebacks that had experienced a more benign environment earlier in life subsequently reduced their investment in carotenoid‐based sexual signals early in the breeding season, and consequently senesced at a slower rate later in the season, compared to those that had developed under harsher conditions. This plasticity of ageing was genetically determined. Both antagonistic pleiotropy and genetic variation in the rate of senescence were evident only in the individuals raised in the harsher environment.The experimental demonstration of genotype‐by‐environment interactions influencing the rate of reproductive senescence provides interesting insights into the role of the environment in the evolution of life histories. The results suggest that benign conditions weaken the scope for senescence to evolve and that the dependence on the environment may maintain genetic variation under selection.

Sex‐specific patterns of reproductive senescence in a long‐lived reintroduced raptor

“…The environment experienced in early life often has an effect on individual condition and the breeding performance or rate of aging in later life (Balbontín & Møller, ; Bouwhuis et al., ; Kim, Metcalfe, & Velando, ). Under experimental conditions, three‐spined stickleback Gasterosteus aculeatus originating from a more benign early life environment senesced at a slower rate than those that experienced a harsh early life environment (Kim et al., ). In the same way, Mitchell, Wellicome, Brodie, and Cheng () found differences in the subsequent breeding performance of reintroduced burrowing owls Athene cunicularia hypugaea subjected to contrasting release methods.…”

Transcriptional mechanisms underlying life‐history responses to climate change in the three‐spined stickleback

“…Body mass of the juvenile fish did not differ between the two treatment groups prior to the temperature manipulation (ln‐transformed body mass at age 6 months; two‐tailed t test: t 1036 = 1.293, p = .196). Water temperature in the warm‐treated tanks was maintained at 14°C during winter, whereas the temperature in the control tanks was gradually reduced from 14°C in November to 9°C in January then increased to 14°C in March, simulating the natural seasonal pattern at the sampling site of the parent fish (Kim et al., ). Some global warming scenarios predict an increase of 4–6°C in average winter water temperature in this latitude (Majone, Bovolo, Bellin, Blenkinsop, & Fowler, ).…”

Early exposure to a bacterial endotoxin advances the onset of moult in the European starling

“…Many studies reported negative fitness effects of early developmental stressors (see Introduction), though a few documented positive effects (Moret and Siva‐Jothy ). Others showed long‐term impacts that are difficult to assess either positively or negatively (Andrews et al , O'Hagan et al , Kim et al ). Among the studies reporting long‐lasting positive effects, one showed that the larvae of the mealworm beetles Tenebrio molitor exposed to LPS increased their resistance against a fungal parasite at the adult stage (Moret and Siva‐Jothy ).…”

“…Among the studies reporting long‐lasting positive effects, one showed that the larvae of the mealworm beetles Tenebrio molitor exposed to LPS increased their resistance against a fungal parasite at the adult stage (Moret and Siva‐Jothy ). In contrast, male three‐spined sticklebacks Gasterosteus aculeatus developed under harsh conditions increased their investment in carotenoid‐based sexual signals which entails positive effects on fitness, but also showed a fast senescence rate (Kim et al ). In starlings, an increased sibling competition, despite not having any detectable effect on nestling growth, caused alterations in flight performance and feeding behaviour later in life (Andrews et al , O'Hagan et al ).…”