The Ecology of Collective Behavior in Ants

Nest choice in Temnothorax spp.; task allocation and the regulation of activity in Pheidole dentata, Pogonomyrmex barbatus, and Atta spp.; and trail networks in Monomorium pharaonis and Cephalotes goniodontus all provide examples of correspondences between the dynamics of the environment and the dynamics of collective behavior. Some important aspects of the dynamics of the environment include stability, the threat of rupture or disturbance, the ratio of inflow and outflow of resources or energy, and the distribution of resources. These correspond to the dynamics of collective behavior, including the extent of amplification, how feedback instigates and inhibits activity, and the extent to which the interactions that provide the information to regulate behavior are local or spatially centralized.

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

Miniaturized nervous systems have been thought to limit behavioral ability, and animals with miniaturized brains may be less flexible when challenged by injuries resulting in sensory deficits that impact the development, maintenance, and plasticity of small-scale neural networks. We experimentally examined how injuries to sensory structures critical for olfactory ability affect behavioral performance in workers of the ant Pheidole dentata, which have minute brains (0.01 mm3) and primarily rely on the perception and processing of chemical signals and cues to direct their social behavior. We employed unilateral antennal denervation to decrease the olfactory perception ability of workers and quantified consequential neuroanatomical and behavioral performance effects. Postablation neuroanatomical metrics revealed a 25% reduction in the volume of the antennal lobe ipsilateral to the antennal lesion relative to the contralateral lobe, indicating atrophy of the input-deprived tissue. However, antennectomy did not affect the volumes of the mushroom body or its subcompartments or the number of mushroom body synaptic complexes (microglomeruli) in either brain hemisphere. Synapsin immunoreactivity, however, was significantly higher in the ipsilateral mushroom body calyces, which could reflect presynaptic potentiation and homeostatic compensation in higher-order olfactory regions. Despite tissue loss caused by antennal lesioning and resulting unilateral sensory deprivation, the ability of workers to perform behaviors that encompass the breadth of their task repertoire and meet demands for colony labor remained largely intact. The few behavioral deficits recorded were restricted to pheromone trail-following ability, a result that was expected due to the need for bilateral olfactory input to process spatial odor information. Our macroscopic and cellular neuroanatomical measurements and assessments of task performance demonstrate that the miniaturized brains of P. dentata workers and their sensorimotor functions are remarkably robust to injury-related size reduction and remain capable of generating behaviors required to respond appropriately to chemical social signals and effectively nurse immatures, as well as participate in coordinated foraging.

A MATHEMATICAL FRAMEWORK EXHIBITING THE EMERGENCE OF DYNAMIC EXPANSION OF TASK REPERTOIRE IN PHEIDOLE DENTATA

The division of labor (DOL) and task allocation (TA) among groups of ants living in a colony is thought to be highly efficient, and key to the robust survival of a colony. A great deal of experimental and theoretical work has been done toward gaining a clear understanding of the evolution of, and underlying mechanisms of these phenomena. Much of this research has utilized mathematical modeling. Here we continue this tradition by developing a mathematical model for a particular aspect of TA, known as age-related repertoire expansion, that has been observed in the minor workers of the ant species Pheidole dentata. In fact, we present a relatively broad mathematical modeling framework based on the dynamics of the frequency with which members of specific age groups carry out distinct tasks. We apply our modeling approach to a specific TA scenario, and compare our theoretical results with experimental data. It is observed that the model predicts perceived behavior, and provides a possible explanation for the aforementioned experimental results.

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.