Rank-related contrasts in longevity arise from extra-group excursions not delayed senescence in a cooperative mammal

Abstract

In many cooperatively breeding animal societies, breeders outlive non-breeding subordinates, despite investing heavily in reproduction. In eusocial insects, the extended lifespans of breeders arise from specialized slowed aging profiles, prompting suggestions that reproduction and dominance similarly defer aging in cooperatively breeding vertebrates, too. Although lacking the permanent castes of eusocial insects, breeders of vertebrate societies could delay aging via phenotypic plasticity (similar rank-related changes occur in growth, neuroendocrinology, and behavior), and such plastic deferment of aging may reveal novel targets for preventing aging-related diseases. Here, we investigate whether breeding dominants exhibit extended longevity and delayed age-related physiological declines in wild cooperatively breeding meerkats. We show that dominants outlive subordinates but exhibit faster telomere attrition (a marker of cellular senescence and hallmark of aging and that in dominants (but not subordinates), rapid telomere attrition is associated with mortality. Our findings further suggest that, rather than resulting from specialized aging profiles, differences in longevity between dominants and subordinates are driven by subordinate dispersal forays, which become exponentially more frequent with age and increase subordinate mortality. These results highlight the need to critically examine the causes of rank-related longevity contrasts in other cooperatively breeding vertebrates, including social mole-rats, where they are currently attributed to specialized aging profiles in dominants.