Abstract
Social experience early in life appears to be necessary for the development of species-typical behavior. Although isolation during critical periods of maturation has been shown to impact behavior by altering gene expression and brain development in invertebrates and vertebrates, workers of some ant species appear resilient to social deprivation and other neurobiological challenges that occur during senescence or due to loss of sensory input. It is unclear if and to what degree neuroanatomy, neurochemistry, and behavior will show deficiencies if social experience in the early adult life of worker ants is compromised. We reared newly-eclosed adult workers of Camponotus floridanus under conditions of social isolation for 2 to 53 days, quantified brain compartment volumes, recorded biogenic amine levels in individual brains, and evaluated movement and behavioral performance to compare the neuroanatomy, neurochemistry, brood-care behavior, and foraging (predatory behavior) of isolated workers with that of workers experiencing natural social contact after adult eclosion. We found that the volume of the antennal lobe, which processes olfactory inputs, was significantly reduced in workers isolated for an average of 40 days, whereas the size of the mushroom bodies, centers of higher-order sensory processing, increased after eclosion and was not significantly different from controls. Titers of the neuromodulators serotonin, dopamine, and octopamine remained stable and were not significantly different in isolation treatments and controls. Brood care, predation, and overall movement were reduced in workers lacking social contact early in life. These results suggest that the behavioral development of isolated workers of C. floridanus is specifically impacted by a reduction in the size of the antennal lobe. Task performance and locomotor ability therefore appear to be sensitive to a loss of social contact through a reduction of olfactory processing ability rather than change in the size of the mushroom bodies, which serve important functions in learning and memory, or the central complex, which controls movement.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
We reorganized our data to limit statistical comparisons to isolation treatment outcomes (neuroanatomy, neurochemistry, and behavior) and age-matched controls (control callows, 2-day isolates) and reasonably estimated age-matched control (40-day isolates and control mature workers). We identified mature workers from their degree of cuticular coloration, which becomes fully pigmented at approximately two-three weeks. We combined 30- and 45- day isolate data into the 40-day isolation group to increase statistical power. In doing so, we validated that 30- and 45- day isolate outcomes were not significantly different. We then placed data on 5- and 20- day isolates lacking age-matched controls into supplementary data to illustrate trajectories of change in neuroanatomy and neurochemistry with increasing isolation.