Neuroanatomical and neurochemical correlates of senescence and social role in the ant Pheidole dentata

Sociality shapes patterns of senescence, evidenced by the remarkable lifespan plasticity of social insect queens and workers. Ants, exemplars of eusociality, provide diverse systems to explore the sociobiology of senescence by examining how sterile workers partition colony labor over their lifespans, and how neurobiological factors affect transitions among social roles and age-related task performance efficacies. Integrating sociobiology, senescence theory, and neurobiology, I examined the relationship of chronological age and social behavior during the ~140-day lifespan of workers of the ant Pheidole dentata. I critically analyzed programmed senescence in respect to the sociobiology of worker longevity and evaluated how large colony size achieved through selection for extended worker lifespan enhances colony fitness. My study found no support for worker programmed senescence. Further testing senescence theory, I determined if workers declined behaviorally as they aged due to increased apoptotic cell death and changes in synaptic complexes associated with higher-order processing in the brain. Using robust behavioral assays I found aging was not correlated with declines in sensory responsiveness or motor functions associated with foraging, nursing, and prey-capture tasks, or activity level and phototaxis. Old minor workers (95 days) followed pheromone trails for greater distances than 20-day old minors and showed higher activity levels, suggesting improvement in behavioral performance. Neural substrates likely underscoring task performance were maintained with age: synaptic complex density was constant and apoptosis was unchanged with age. Sensory and motor control brain regions did not show age-related increases in neurodegeneration. Worker spatial location predicted social role independent of age: foragers exhibited higher activity levels and more aggressive predatory behavior than nurses. Serotonin and dopamine titers increased from 20 to 120 days but showed no clear correlation with social role. Pharmacological manipulations of brain serotonin had no effect on brood care, predatory response, activity, or phototaxis. Finally, I assessed arborization of a serotonergic neuron hypothesized to underscore task performance to determine how aging across subcastes influences neuronal structure. Major workers showed greater branching complexity than minors and an age-related increase in arbor complexity. P. dentata workers appear to show negligible behavioral and neural senescence throughout their lifespans

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

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

Lifespan behavioural and neural resilience in a social insect

International audienceAnalyses 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

Data from: Lifespan behavioral 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

Brood care acts

Brood care act

Brood care time

Brood care tim

Trail following

Annulus half width indicates the half width of the area around the pheromone trail where ants were tracked