The metabolic expense of producing and operating neural tissue required for adaptive behaviour is considered a significant selective force in brain evolution. In primates, brain size correlates positively with group size, presumably owing to the greater cognitive demands of complex social relationships in large societies. Social complexity in eusocial insects is also associated with large groups, as well as collective intelligence and division of labour among sterile workers. However, superorganism phenotypes may lower cognitive demands on behaviourally specialized workers resulting in selection for decreased brain size and/or energetic costs of brain metabolism. To test this hypothesis, we compared brain investment patterns and cytochrome oxidase (COX) activity, a proxy for ATP usage, in two ant species contrasting in social organization. Socially complex Oecophylla smaragdina workers had larger brain size and relative investment in the mushroom bodies (MBs)-higher order sensory processing compartments-than the more socially basic Formica subsericea workers. Oecophylla smaragdina workers, however, had reduced COX activity in the MBs. Our results suggest that as in primates, ant group size is associated with large brain size. The elevated costs of investment in metabolically expensive brain tissue in the socially complex O. smaragdina, however, appear to be offset by decreased energetic costs.

The social brain hypothesis predicts that larger group size and greater social complexity select for increased brain size. In ants, social complexity is associated with large colony size, emergent collective action, and division of labor among workers. The great diversity of social organization in ants offers numerous systems to test social brain theory and examine the neurobiology of social behavior. My studies focused on the Australasian weaver ant, Oecophylla smaragdina, a polymorphic species, as a model of advanced social organization. I critically analyzed how biogenic amines modulate social behavior in ants and examined their role in worker subcaste-related territorial aggression. Major workers that naturally engage in territorial defense showed higher levels of brain octopamine in comparison to more docile, smaller minor workers, whose social role is nursing. Through pharmacological manipulations of octopaminergic action in both subcastes, octopamine was found to be both necessary and sufficient for aggression, suggesting subcaste-related task specialization results from neuromodulation. Additionally, I tested social brain theory by contrasting the neurobiological correlates of social organization in a phylogenetically closely related ant species, Formica subsericea, which is more basic in social structure. Specifically, I compared brain neuroanatomy and neurometabolism in respect to the neuroecology and degree of social complexity of O. smaragdina major and minor workers and F. subsericea monomorphic workers. Increased brain production costs were found in both O. smaragdina subcastes, and the collective action of O. smaragdina majors appeared to compensate for these elevated costs through decreased ATP usage, measured from cytochrome oxidase activity, an endogenous marker of neurometabolism. Macroscopic and cellular neuroanatomical analyses of brain development showed that higher-order sensory processing regions in workers of O. smaragdina, but not F. subsericea, had age-related synaptic reorganization and increased volume. Supporting the social brain hypothesis, ecological and social challenges associated with large colony size were found to contribute to increased brain size. I conclude that division of labor and collective action, among other components of social complexity, may drive the evolution of brain structure and function in compensatory ways by generating anatomically and metabolically plastic mosaic brains that adaptively reflect cognitive demands of worker task specialization and colony-level social organization.

What selective forces and molecular mechanisms govern the integration of worker body size and morphology, brain architecture, and behavior in insect societies? Workers of the remarkably polyphenic and socially complex fungus-growing leafcutter ant Atta cephalotes exhibit a striking agricultural division of labor. The number of morphologically distinct and behaviorally differentiated worker groups, adaptive mosaic neural phenotypes, and brain transcriptomes have not been examined and the influences of socioecological challenges on behavioral performance, cognition, and brain evolution are unclear. We quantified worker morphological and behavioral variation to assess the number of worker size classes and characterized their social roles. We discriminated multiple worker size groups using a Gaussian mixture model: mid-sized workers (“medias”) had the most diverse task repertories and serve dominant roles in leaf harvesting, whereas workers of other size classes performed fewer, more specialized behaviors. We used variation among tasks in sensorimotor functions and task performance frequencies to create an estimate of sensory integration and processing demands across worker size groups. This metric predicted that medias require the greatest neural investment due to the high diversity of sensory inputs and motor functions associated with their task set. We quantified the volumes of key neuropils in brains of workers of different sizes and determined their allometries, finding that our estimate corresponded to proportional investment in the mushroom bodies, a brain compartment responsible for learning, memory, and sensory integration, and identifying allometric scaling patterns in other brain centers. Additionally, we measured whole-brain gene expression and identified significant differences in expression levels for numerous genes likely to underpin behavior. Differences were most pronounced between the smallest (fungal gardener “minims”) and largest (defensive “majors”), although not all expression differences were driven by worker size. Overrepresented gene functional categories included those related to sensory processing (enriched in genes upregulated in medias and minims) and metabolism (enriched in genes upregulated in majors). These results identify the nature of selective forces favoring differentiation along morphological, neuroanatomical, behavioral, and molecular axes among A. cephalotes workers and the impact of advanced division of labor on brain evolution. / 2023-03-01T00:00:00Z