Molecular Tuning and Morphology of the Olfactory System Underlie Nestmate Recognition in a Polymorphic Ant

Ants, the largest hymenopteran family of social insects, have evolved complex societies characterised by a reproductive division of labour between morphologically distinct reproductive (queen) and worker castes. Many ant species have monomorphic workers, with all individuals sharing similar size and shape. Other ant species comprise polymorphic workers that differ in size and shape, traits associated with specialised roles within the colony. One such role is nestmate recognition, an essential task which maintains the integrity of the society by preventing unrelated individuals from exploiting the colony's resources. The ability to detect nestmates and non-nestmates relies on discriminating among cuticular hydrocarbon (CHC) blends, which are colony specific. This process involves a dedicated olfactory recognition system, which includes specialised antennal sensilla and specific olfactory receptor (OR) genes, both associated with a particular region in the primary olfactory processing centre of the brain, the antennal lobe. Using the highly polymorphic harvester ant, Messor barbarus, we employed a multidisciplinary approach, including electron microscopy, transcriptomics, behavioural analyses and neuroanatomy, to investigate whether nestmate recognition differs among different worker morphs and how this might correlate with specific features of the olfactory system. We demonstrate that small workers exhibit strong nestmate recognition and that this ability aligns with differences in the olfactory system, including an increased proportion of basiconic sensilla and the overexpression of certain 9-exon OR genes. Our study elucidates how social insect workers may differ at the behavioural, morphological and genetic level giving rise to task specialisation within the colony.