Genetic basis of chemical communication in eusocial insects

Abstract

Social behavior is one of the most fascinating and complex behaviors in humans and animals. A fundamental process of social behavior is communication among individuals. It relies on the capability of the nervous system to sense, process, and interpret various signals (e.g., pheromones) and respond with appropriate decisions and actions. Eusocial insects, including ants, some bees, some wasps, and termites, display intriguing cooperative social behavior. Recent advances in genetic and genomic studies have revealed key genes that are involved in pheromone synthesis, chemosensory perception, and physiological and behavioral responses to varied pheromones. In this review, we highlight the genes and pathways that regulate queen pheromone-mediated social communication, discuss the evolutionary changes in genetic systems, and outline prospects of functional studies in sociobiology.

Keywords: chemosensory system; communication; genetic regulation; pheromone; signal evolution; social behavior.

Figure 1.

Sender-precursor model for the evolution of pheromones. An unselected cue that is secreted by a sender and is associated with a condition of the sender is sensed by a receiver through its olfactory system. If the receiver benefits from the information about the sender's condition, the receiver's olfactory system and higher brain centers are selected for better discrimination with associated changes in physiology and behavior. Conversely, if the sender benefits from the receiver's response, the cue is now under selection and becomes a chemical signal (pheromone) used for communication. This leads to a positive feedback loop with selection for a stronger and clearer signal in the sender (ritualization) and better discrimination by the receiver until costs of further modifications outweigh the benefits of signal ritualization and/or receiver adaptations.

Figure 2.

Pheromone production, perception, and its induced responses. (Top panel) The precursors of sender's QMP and CHC pheromones, normally 16- to 20-carbon fatty acyl-CoA (or fatty acid), are synthesized from acetyl-CoA, the multistep reactions catalyzed by fatty acid synthase (FAS) and other enzymes. QMP synthesis is catalyzed by enzymes such as cytochrome P450 mono-oxygenases and alcohol dehydrogenases (ADHs), while CHC synthesis is catalyzed by cytochrome P450, elongases, and desaturases. The most common forms of CHC pheromones are alkanes (saturated) and methyl-alkanes, and alkenes (unsaturated). (Middle panel) Pheromones are sensed primarily by the receiver's odorant receptors (ORs) expressed in peripheral neurons (ORNs), whose dendrites are located in the sensillum, and axons project to glomeruli in the antennal lobe (AL). The OR genes and number of glomeruli have been expanded in the evolution of hymenopteran insects, notably in those organized in societies. The signal is further processed in the mushroom bodies (MB), the lateral horn (LH), and the central brain. (OL) Optic lobe. (Bottom panel) The altered neuronal activity in the brain may cause the secretion of neurotransmitters, biogenic amines, and hormones, leading to systemic changes in physiology (e.g., reproduction and pheromone synthesis) and behavior in the receiver.