Polyphenism predicts actuarial senescence and lifespan in tiger salamanders

Abstract

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.