Lifespan behavioural and neural resilience in a social insect

Abstract

Analyses of senescence in social species are important to understanding how group living influences the evolution of ageing in society members. Social insects exhibit remarkable lifespan polyphenisms and division of labour, presenting excellent opportunities to test hypotheses concerning ageing and behaviour. Senescence patterns in other taxa suggest that behavioural performance in ageing workers would decrease in association with declining brain functions. Using the ant Pheidole dentata as a model, we found that 120-day-old minor workers, having completed 86% of their laboratory lifespan, showed no decrease in sensorimotor functions underscoring complex tasks such as alloparenting and foraging. Collaterally, we found no age-associated increases in apoptosis in functionally specialized brain compartments or decreases in synaptic densities in the mushroom bodies, regions associated with integrative processing. Furthermore, brain titres of serotonin and dopamine-neuromodulators that could negatively impact behaviour through age-related declines-increased in old workers. Unimpaired task performance appears to be based on the maintenance of brain functions supporting olfaction and motor coordination independent of age. Our study is the first to comprehensively assess lifespan task performance and its neurobiological correlates and identify constancy in behavioural performance and the absence of significant age-related neural declines.

Behavioral Performance and Neural Systems Are Robust to Sensory Injury in Workers of the Ant Pheidole dentata

“…It is notable that in our experimental study reducing the size of a minute brain by 25%, while causing significant changes in trail following ability, did not significantly compromise worker performance in other task assays, including our comprehensive assessment of the ability of workers to forage for and tend to larvae. Adult neurogenesis, which could compensate for neuron loss, is not thought to occur in adult hymenopterans [Fahrbach et al, 1995;Gronenberg et al, 1996;Cayre et al, 2002], but the brains of P. dentata workers nevertheless remain functionally robust following antennal lesioning as well as throughout much of the minor worker lifespan [Giraldo et al, 2016]. The maintenance of MB architecture, as we demonstrated, may allow workers to remain adept at task performance.…”

“…It is of interest that this module is robust to injury, enabling social functions to be maintained following a substantial reduction in sensory input. Giraldo et al [2016] hypothesized that P. dentata worker brains allocate energy savings toward neuromolecular mechanisms that decrease apoptosis, increase brain monoamine levels, and thus prevent behavioral senescence. Our present finding of increased synapsin immunoreactivity after lesioning could be in part associated with accommodation in sensorimotor function.…”

“…To quantify MG in worker MB, brains were processed as described by Giraldo et al [2016]. Brains were dissected in cold HEPES-buffered saline and fixed overnight in 4% paraformaldehyde.…”

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).…”

Conserved regulators of cognitive aging: From worms to humans

“…Moreover, a vast number of genetic techniques and tools are available that allow precise spatial and temporal control of genetic perturbations [38, 129]. Other invertebrate species, such as ants and bees, show promise for future studies in aging and cognition, but in the present review, the focus will be on more commonly used, genetically tractable organisms [4, 8, 36, 37, 66]. Though these features make invertebrate models attractive in the study of aging, there are some obvious caveats when working in such a simple system.…”