An exploration of the social brain hypothesis in insects

Abstract

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.

Keywords: cognition; insects; mushroom bodies; social brain hypothesis; sociality.

Figure 1

Comparing insect brain sizes. (A) Schematic drawing of a honeybee worker brain (Apis mellifera). The visual lobes (VL) composed of the lamina (La), the medulla (Me), and the lobula (Lo), receive the sensory inputs from the compound eyes. The antennal lobes (AL) receive the inputs from the olfactory sensory neurons of the antennae in spherical subunits (glomeruli) that represent particular aspects of an odor. The mushroom bodies are central structures that process multimodal information and participate in learning and memory. These structures have a characteristic morphology consisting of a pedunculus (Pe) and two calyces (Ca) compartmentalized into the lip (l), which receives olfactory input from the antennal lobes (blue neural network), the collar (c), which receives input from the visual lobes (red neural network), and the basal ring (b), which receives combined input from the antennal and visual lobes. The central body (CB) has connections to all major parts of the brain and is involved in leg coordination and motor control. Image modified from Menzel and Giurfa (2001). (B) Schematic representation of the morphology of the mushroom bodies of Hymenoptera, mapped on a simplified phylogeny, based on Farris and Schulmeister (2011). The mushroom bodies of phytophageous lineages are small, the calyces lack subcompartmentalization and do not receive visual inputs from the optic lobes. Large mushroom bodies with lip, collar and basal ring subcompartments in the calyx, and visual inputs arose concurrent with the acquisition of a parasitoid mode of life at the base of the Euhymenopteran, ca 90My prior to the evolution of social aculeates, such as honeybees.

Figure 2

Examples of socio-cognitive tasks by social insects that might involve computationally inexpensive cognition and minor adjustment of neural circuitry. (A) In small colonies of the wasps Polistes fuscatus, cooperatively breeding females learn the identity of every other females based on their conspicuous facial markings. Face recognition helps stabilize social interactions and reducing aggressions (photos M. J. Sheehan). (B) Each colony of the Brazilian stingless bee Partamona pearsoni marks its nest entrance with a visually unique structure, which defines the colony’s identity. Using colony-specific identifiers, a society can theoretically become infinitely large without increasing the cognitive demands on its members (photo J. M. F. Camargo). (C) Honeybees, such as Apis florea, communicate food and potential nest locations to their nestmates using a “dance” language. Upon its return to the nest, a successful forager performs a figure-of-eight-shaped circuit (white arrows) conveying information about the distance (duration of the waggle phase) and the direction (body orientation relative to gravity) of the target resource (photo J. Makinson). (D) The Australian termites Nasutitermes triodiae build complex “cathedral” nests several meters high containing multiple chambers. Walls and pillars arise through the action of many termites, each depositing soil pellets at sites scented with an attractive cement pheromone, which coordinates the accumulation of building materials without any individual having a global knowledge of the construction process (photo S. Scheurer). (E) Argentine ants Linepithema humile develop pheromone transportation networks to connect the multiple nests of the colony. Collectively, ants establish near optimal networks using pheromone trails as an “externalized memory” (photo T. Latty).