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 [1-3]. In eusocial insects, the extended lifespans of breeders arise from specialized slowed aging profiles [1], prompting suggestions that reproduction and dominance similarly defer aging in cooperatively breeding vertebrates, too [4-6]. 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 [7-10]), and such plastic deferment of aging may reveal novel targets for preventing aging-related diseases [11]. 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 [12]) 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 [4].

The importance of being beta: female succession in a cooperative breeder

“…This appears to be due natal dominants also losing dominance at an earlier age, which as dominance tenures most commonly end in death suggests that the fate of dominants is determined by a maximum dominance span not a maximum life span. This is in line with evidence of the cumulative physiological costs of dominance and reproduction (Blount, Vitikainen, Stott, & Cant, 2016;Cram, Blount, & Young, 2015;Sapolsky, 2005) and supports recent analysis of meerkats showing dominant mortality being driven by accelerated senescence (Cram et al, 2018). This is likely why even though the availability of different routes to dominance vary with age, the fitness benefits do not differ between them.…”

Sex‐independent senescence in a cooperatively breeding mammal

“…In meerkats, tuberculosis represents a possible mechanism by which terminal declines might be mediated, and anecdotally, individuals reaching an advanced stage of morbidity through tuberculosis exposure display dramatic reductions in body mass, dying shortly afterwards. The telomeres of meerkats also shorten rapidly in the period immediately prior to death (Cram et al, 2018). A broader examination of physiological changes across the lifespan would no doubt identify further markers of bodily decline associated with age-dependent and age-independent mass variation (e.g.…”

“…One possible explanation relates to group living. Incumbent dominants can maintain long tenures sheltered from extrinsic mortality in large groups with dedicated sentinels (Cram et al, 2018), and this buffering effect of group living might be enough to prevent age-dependent increases in mortality risk in dominants irrespective of individual declines in condition. Alternatively, the presence and intensity of survival senescence might vary over time as environmental and demographic conditions modify the likelihood of different forms of intrinsic and extrinsic mortality (Berger, Lemaître, Allainé, Gaillard, & Cohas, 2018;Hämäläinen et al, 2014;Ronget, Garratt, Lemaître, & Gaillard, 2017), and might go undetected when these sources of variation are not accounted for in survival analyses.…”

“…In meerkats, reproduction is monopolized by a dominant male and a dominant female in each group (Clutton-Brock & Manser, 2016) with subordinate individuals of both sexes helping to protect and feed juveniles born in the group. Only a small proportion of individuals ever acquire dominance (Duncan, Gaynor, & Clutton-Brock, 2018;Spong, Hodge, Young, & Clutton-Brock, 2008), with those that are unsuccessful in doing so experiencing an increasing mortality risk that is associated with extended periods of time spent away from the natal group beyond 1.5 years of age (Cram et al, 2018). As a result, subordinate individuals have shorter longevities than dominants so that the potential to detect senescence in subordinate individuals is limited (Sharp & Clutton-Brock, 2010).…”

Wandering woodpeckers: foray behavior in a social bird

“…Forays provide critical social information and improve dispersal outcomes (Conradt et al ). Yet, depending on their spatial extent, forays can be energetically costly and physiologically stressful (Young and Monfort , Cram et al ), and intruding individuals are often expelled aggressively by resident territory holders, prompting foraying individuals to be behaviorally cryptic (Eikenaar et al ). Forays thus entail a trade‐off between physiological and energetic costs versus improved dispersal and fitness outcomes.…”