Lifespan behavioural and neural resilience in a social insect.

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.

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

Social insect workers modify task performance according to age-related schedules of behavioral development, and/or changing colony labor requirements based on flexible responses that may be independent of age. Using known-age minor workers of the ant Pheidole dentata throughout 68% of their 140-day laboratory lifespan, we asked whether workers found inside or outside the nest differed in task performance and if behaviors were correlated with and/or causally linked to changes in brain serotonin (5HT) and dopamine (DA). Our results suggest that task performance patterns of individually assayed minors collected at these two spatially different worksites were independent of age. Outside-nest minors displayed significantly higher levels of predatory behavior and greater activity than inside-nest minors, but these groups did not differ in brood care or phototaxis. We examined the relationship of 5HT and DA to these behaviors in known-age minors by quantifying individual brain titers. Both monoamines did not increase significantly from 20 to 95 days of age. DA did not appear to directly regulate worksite location, although titers were significantly higher in outside-nest than inside-nest workers. Pharmacological depletion of 5HT did not affect nursing, predation, phototaxis or activity. Our results suggest that worker task capabilities are independent of age beyond 20 days, and only predatory behavior can be consistently predicted by spatial location. This could reflect worker flexibility or variability in the behavior of individuals collected at each location, which could be influenced by complex interactions between age, worksite location, social interactions, neuromodulators, and other environmental and internal regulators of behavior.