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Abstract Actuarial senescence (called ‘senescence’ hereafter) often shows broad variation at the intraspecific level. Phenotypic plasticity likely plays a central role in among‐individual heterogeneity in senescence rate (i.e. the rate of increase in mortality with age), although our knowledge on this subject is still very fragmentary. Polyphenism—the unique sub‐type of phenotypic plasticity where several discrete phenotypes are produced by the same genotype—may provide excellent study systems to investigate if and how plasticity affects the rate of senescence in nature.In this study, we investigated whether facultative paedomorphosis influences the rate of senescence in a salamander,Ambystoma mavortium nebulosum. Facultative paedomorphosis, a unique form of polyphenism found in dozens of urodele species worldwide, leads to the production of two discrete, environmentally induced phenotypes: metamorphic and paedomorphic individuals. We leveraged an extensive set of capture–recapture data (8948 individuals, 24 years of monitoring) that were analysed using multistate capture–recapture models and Bayesian age‐dependent survival models.Multistate models revealed that paedomorphosis was the most common developmental pathway used by salamanders in our study system. Bayesian age‐dependent survival models then showed that paedomorphs have accelerated senescence in both sexes and shorter adult lifespan (in females only) compared to metamorphs. In paedomorphs, senescence rate and adult lifespan also varied among ponds and individuals. Females with good body condition and high lifetime reproductive success had slower senescence and longer lifespan. Late‐breeding females also lived longer but showed a senescence rate similar to that of early‐breeding females. Moreover, males with good condition had longer lifespan than males with poor body condition, although they had similar senescence rates. In addition, late‐breeding males lived longer but, unexpectedly, had higher senescence than early‐breeding males.Overall, our work provides one of the few empirical cases suggesting that environmentally cued polyphenism could affect the senescence of a vertebrate in nature, thus providing insights on the ecological and evolutionary consequences of developmental plasticity on ageing. 

Abstract Fitness trade‐offs are a foundation of ecological and evolutionary theory because trade‐offs can explain life history variation, phenotypic plasticity, and the existence of polyphenisms.Using a 32‐year mark‐recapture dataset on lifetime fitness for 1093 adult Arizona tiger salamanders (Ambystoma mavortium nebulosum) from a high elevation, polyphenic population, we evaluated the extent to which two life history morphs (aquatic paedomorphs vs. terrestrial metamorphs) exhibited fitness trade‐offs in breeding and body condition with respect to environmental variation (e.g. climate) and internal state‐based variables (e.g. age).Both morphs displayed a similar response to higher probabilities of breeding during years of high spring precipitation (i.e. not indicative of a morph‐specific fitness trade‐off). There were likely no climate‐induced fitness trade‐offs on breeding state for the two life history morphs because precipitation and water availability are vital to amphibian reproduction.Body condition displayed a contrasting response for the two morphs that was indicative of a climate‐induced fitness trade‐off. While metamorphs exhibited a positive relationship with summer snowpack conditions, paedomorphs were unaffected. Fitness trade‐offs from summer snowpack are likely due to extended hydroperiods in temporary ponds, where metamorphs gain a fitness advantage during the summer growing season by exploiting resources that are unavailable to paeodomorphs. However, paedomorphs appear to have the overwintering fitness advantage because they consistently had higher body condition than metamorphs at the start of the summer growing season.Our results reveal that climate and habitat type (metamorphs as predominately terrestrial, paedomorphs as fully aquatic) interact to confer different advantages for each morph. These results advance our current understanding of fitness trade‐offs in this well‐studied polyphenic amphibian by integrating climate‐based mechanisms. Our conclusions prompt future studies to explore how climatic variation can maintain polyphenisms and promote life history diversity, as well as the implications of climate change for polyphenisms.