The evolution and organization of non-canonical olfactory systems in ants and other insects

Susanne Foitzik – Universität Mainz
Hugo Darras – Universität Mainz
Carlotta Martelli – Universität Mainz

Odorant Receptors (ORs) constitute the main family of chemosensory genes in nearly all species. Based on the canonical model of the olfactory circuit, a single OR is expressed in each Olfactory Receptor Neuron (ORN), which projects to a single OR-specific glomerulus in the brain. ORs are fast evolving gene families that underwent frequent expansions and contractions to facilitate adaptation to different ecological needs and the evolution of insect societies. This poses a fundamental challenge to the evolution of olfactory neural circuits, which should occur in parallel to that of OR gene families to maintain the canonical ‘OR-ORN-glomerulus’ scheme. Recent studies on ants and mosquitoes suggest that this canonical model might not be universal. By combining brain anatomical and transcriptome analyses, we have shown that workers of the ant Temnothorax longispinosus exhibit multifold variation in the number of glomeruli in their antennal lobes, despite expressing almost all OR genes in their antennae. Together with previous studies, this suggests the existence of different mechanisms for the development of the olfactory system in ants and adds possible variants of neural circuit architecture found for olfaction across insect taxa. In this project, our first aim is to understand the organizational logic of the olfactory system of T. longispinosus from genes to neurons by linking OR genomic organization and expression patterns. Second, we aim at relating individual variation in brain anatomy to the behavioral role of a worker in her colony to unveil functional consequences of inter-individual variation. Next, we will investigate whether interindividual anatomical variation also occur in other ant and insect species, with the long-term goal of characterizing the evolutionary origin and function of such variation. Finally, we will implement a theoretical approach to understand which computational principles favor a non-canonical, and perhaps individualized, architecture of the olfactory system and to develop a minimum evolutionary model that explains the diversity of olfactory systems. Our approach combines genomic, molecular, neurobiological, comparative, and computational methods to link genome architecture to neural circuit architecture and to understand the functional consequences and evolutionary origin of the diversity of olfactory circuit organization.