Worker senescence and the sociobiology of aging in ants

Abstract

Senescence, the decline in physiological and behavioral function with increasing age, has been the focus of significant theoretical and empirical research in a broad array of animal taxa. Preeminent among invertebrate social models of aging are ants, a diverse and ecologically dominant clade of eusocial insects characterized by reproductive and sterile phenotypes. In this review, we critically examine selection for worker lifespan in ants and discuss the relationship between functional senescence, longevity, task performance, and colony fitness. We did not find strong or consistent support for the hypothesis that demographic senescence in ants is programmed, or its corollary prediction that workers that do not experience extrinsic mortality die at an age approximating their lifespan in nature. We present seven hypotheses concerning how selection could favor extended worker lifespan through its positive relationship to colony size and predict that large colony size, under some conditions, should confer multiple and significant fitness advantages. Fitness benefits derived from long worker lifespan could be mediated by increased resource acquisition, efficient division of labor, accuracy of collective decision-making, enhanced allomaternal care and colony defense, lower infection risk, and decreased energetic costs of workforce maintenance. We suggest future avenues of research to examine the evolution of worker lifespan and its relationship to colony fitness, and conclude that an innovative fusion of sociobiology, senescence theory, and mechanistic studies of aging can improve our understanding of the adaptive nature of worker lifespan in ants.

Lifespan behavioural and neural resilience in a social insect

“…Social insect workers have been hypothesized to experience programmed death at an age marginally greater than their life expectancy in nature [66], implying that task performance abilities either gradually diminish or abruptly decline with age. Although worker longevity in the field is not known in P. dentata, it is reasonably anticipated to be shorter than the 140-day lifespan we recorded in the laboratory, given increased worker mortality associated with the transition to extranidal tasks performed in more unpredictable environments [20,67,68]. Although we cannot exclude the possibility that P. dentata minor workers decline rapidly just before death, this appears to be unlikely because precipitous senescence [69] is rare and associated with unusually high investment in reproduction [70], which is absent in sterile workers.…”

“…Social interactions appear to mediate metabolic homeostasis and affect mortality rates [74]. Division of labour could in part lead to selection for the maintenance of individual functionality throughout the sterile worker lifespan [20]. In ants, specialized morphologies and task performance are key to social complexity; worker polymorphism, task repertoire development and behavioural specialization are underscored by brain neuropil growth and investment patterns [31].…”

“…Few studies have examined the influence of sociality on ageing and life history [11][12][13], and little is understood about cognitive decline and neurobiological changes accompanying senescence in social animals, apart from humans [12,[14][15][16]. Social insects have striking lifespan polyphenisms [17][18][19][20]: queens often live more than a decade, whereas workers may live only several months [21], indicating that the differentiation of reproductive and sterile castes has had profound effects on senescence, which may be influenced by the social organization of colony labour. The relationship of task performance to age-related changes in the worker brain, however, is not well understood.…”

The influence of colony traits on the collective behaviour ofMyrmica scabrinodisants

“…Moreover, adult individuals require mainly carbohydrate diet for energy (Dussutour & Simpson, 2009), so the larger the number of workers, the larger is the amount of carbohydrates needed. On the other hand, because younger ants accomplish tasks inside the nest, having a majority of older individuals in the colony means possessing a greater number of members ready to go outside and able to fulfil riskier tasks (Moro n et al, 2008;Giraldo & Traniello, 2014). Colonies with more old foragers could have some advantage, as workers had time to acquire important information about the colony state and the position of food sources in its surroundings (Herbers & Choiniere, 1996;Giraldo & Traniello, 2014).…”

Age, worksite location, neuromodulators, and task performance in the ant Pheidole dentata

“…or on tasks performed by foragers (Schmid-Hempel and Schmid-Hempel 1984; Burd 1996; Wolf 2008; Grüter et al 2011; Arnan et al 2011). Few studies have considered worker aging and long-term patterns of task performance across the worker lifespan in ants (Lenoir 1979; Mersch et al 2013; Giraldo and Traniello 2014; Giraldo et al 2016). Furthermore, the regulation of task performance involves mechanisms of neural organization that may vary with worker age (Muscedere et al 2011; Stieb et al 2012; Giraldo et al 2013) and be controlled by biogenic amines (Schulz and Robinson 2001; Seid and Traniello 2005; Jones et al 2009; Muscedere and Traniello 2012; Muscedere et al 2013, 2016; Kamhi and Traniello 2013; Smith et al 2013; Kamhi et al 2015).…”