Ant phylogenomics reveal a natural selection hotspot preceding the origin of advanced eusociality

The evolution of sociality has allowed ants to become one of the most conspicuous and ecologically dominant groups of organisms in the world. By sequencing 65 ant genomes, including at least one species from each of the 17 ant subfamilies and 22 non-formicoid species, we successfully resolved the controversial rooting of the ant phylogeny. Moreover, our genomic analyses revealed that the key genetic innovations leading to advanced eusociality occurred during the emergence of the formicoids, the ant clade exhibiting the most advanced forms of reproductive division of labour, caste specialisation and extended queen longevity. This transition was accompanied by an exceptional number of positive selection events. Importantly, the top three gene functions under selection are directly linked to key features of advanced eusociality with histone acetylation being implicated in caste differentiation, gene silencing by RNA in worker sterility and autophagy in longevity. These results show that key pathways associated with eusociality have been under strong selection during the Cretaceous, suggesting that the molecular foundations of advanced eusociality were rapidly acquired by the formicoid common ancestor in less than 20 Ma.