Ancestral complexity and constrained diversification of the ant olfactory system.

Abstract

Communication is a cornerstone of social living, allowing the exchange of information to align goals and synchronize behaviour. Ants, a group of highly successful social insects, have heightened olfactory abilities that are integral to their evolutionary success. Essential for colony cohesion and cooperation, a female-specific olfactory subsystem processes information about nestmate recognition cues (cuticular hydrocarbons), including basiconic sensilla on the antenna and a cluster of specific glomeruli in the antennal lobe. While it has often been linked to ants' social lifestyle, the evolutionary origins and phylogenetic distribution of this system remain unknown. We conducted a comparative exploration of the ant olfactory system across eight major subfamilies, integrating neuroanatomical, chemical and behavioural analyses. Our findings reveal that sophistication of the ant olfactory system has deep evolutionary roots. Moreover, antennal lobe investment is not associated with social traits such as colony size, polygyny or foraging strategies, but correlates with cuticular hydrocarbon profile complexity. Despite neuroanatomical differences, different ant species consistently excel in nestmate discrimination, indicating adaptation to chemical diversity while maintaining reliable social recognition. This suggests that cuticular hydrocarbon profile and neuronal investment in olfactory neuropil have co-evolved to sustain discrimination performance.