Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae)

The olfactory nervous system of insects and mammals exhibits many similarities, which suggests that the mechanisms for olfactory learning may be shared. Molecular genetic investigations of Drosophila learning have uncovered numerous genes whose gene products are essential for olfactory memory formation. Recent studies of the products of these genes have continued to expand the range of molecular processes known to underlie memory formation. Recent research has also broadened the neuroanatomical areas thought to mediate olfactory learning to include the antennal lobes in addition to a previously accepted and central role for the mushroom bodies. The roles for neurons extrinsic to the mushroom body neurons are becoming better defined. Finally, the genes identified to participate in Drosophila olfactory learning have conserved roles in mammalian organisms, highlighting the value of Drosophila for gene discovery.

Wasps (Vespidae) exhibit a range of social complexity, from solitary living to eusocial colonies, and thus are exemplary for studies of the evolutionary origin and maintenance of social behavior in animals. Integral to the definition of eusociality is the presence of reproductive castes, group members that differ qualitatively in their ability to reproduce in a social setting. Behavioral and morphological evidence suggests that caste determination, the developmental process by which differences in fecundity are established, occurs to a large extent before adult emergence (pre-imaginally) in many species of Vespidae, in both basal and advanced taxa within the clade (Vespinae+Polistinae), which includes most eusocial species. Pre-imaginal determination has been documented in many taxa (e.g. independent-founding Polistinae) where it was not thought to occur. Correlative and experimental studies indicate that differences in nutrition during larval development are often the basis of pre-imaginal caste determination. Pre-imaginal caste determination has important implications for the roles of subfertility and manipulation by nest mates in the evolution of eusocial behavior.

The “social brain hypothesis” posits that the cognitive demands of sociality have driven the evolution of substantially enlarged brains in primates and some other mammals. Whether such reasoning can apply to all social animals is an open question. Here we examine the evolutionary relationships between sociality, cognition, and brain size in insects, a taxonomic group characterized by an extreme sophistication of social behaviors and relatively simple nervous systems. We discuss the application of the social brain hypothesis in this group, based on comparative studies of brain volumes across species exhibiting various levels of social complexity. We illustrate how some of the major behavioral innovations of social insects may in fact require little information-processing and minor adjustments of neural circuitry, thus potentially selecting for more specialized rather than bigger brains. We argue that future work aiming to understand how animal behavior, cognition, and brains are shaped by the environment (including social interactions) should focus on brain functions and identify neural circuitry correlates of social tasks, not only brain sizes.