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

Abstract

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.