Adaptive evolution of odorant receptors is associated with elaborations of social organization in ants

Cooperation in social insect colonies depends on a complex vocabulary of chemical signals, which requires a correspondingly complex array of chemosensory receptors. In the genomes of ants, the odorant receptor (OR) gene family is dramatically expanded compared to other insects. This is most notable in the “9-exon” OR subfamily, which was implicated in responding to cuticular hydrocarbons, a major class of signalling compounds. The compilation of a large, high-quality ant genome dataset by the Global Ant Genomics Alliance allows investigating ant OR evolution in unprecedented detail. By analysing 55,068 ORs of 163 representative ant species, we tested for association between the development of sociobiological traits and adaptive evolution of ORs. We provide a detailed analysis of gene family expansions and adaptive sequence evolution at the OR subfamily level, allowing focused analysis of distinct ant lineages. We identified strong enrichment of positive selection on 9-exon ORs in the ancestor of the formicoid clade, the largest clade comprising 90% of the extant ants. Formicoid species are characterized by greater colony size and reproductive division of labour. Thus, our results support a key role of adaptive diversification of chemical communication systems for the evolution of more complex elaboration of social organization in ants. We also observed enrichment of positive selection on 9-exon ORs associated with the more recent evolution of continuous worker polymorphism in multiple lineages. Surprisingly, the recent evolution of other sociobiological traits was associated with depletion of positive selection on ORs. These results suggest that the evolution of worker polymorphism involves more extensive adaptation of chemical communication compared to other aspects of ant sociobiology. Our analysis of an unprecedented ant OR dataset offers new insights into the specific context in which ORs played a major role in the evolution of elaborations in social traits across the diverse phylogeny of ants.