Chemical communication of queen supergene status in an ant

Abstract

Traits of interest to evolutionary biologists often have complex genetic architectures, the nature of which can confound traditional experimental study at single levels of analysis. In the fire ant Solenopsis invicta, the presence of a Mendelian 'supergene' is both necessary and sufficient to induce a shift in a fundamental property of social organization, from single-queen (monogyne) to multiple-queen (polygyne) colonies. This selfish genetic element, termed the Social b (Sb) supergene, contains > 600 genes that collectively promote its fitness by inducing the characteristic polygyne syndrome, in part by causing polygyne workers to accept only queens bearing the Sb element (a behaviour termed 'worker Sb discrimination'). Here, we employ a newly developed behavioural assay to reveal that polygyne workers, many of which bear the Sb element, employ chemical cues on the cuticle of queens to achieve worker Sb discrimination, but we found no evidence for such pheromonally mediated worker Sb discrimination in monogyne workers, which universally lack the Sb element. This polygyne worker Sb discrimination was then verified through a 'green beard' effect previously described in this system. We thus have demonstrated that the Sb element is required both for production of relevant chemical cues of queens and for expression of the behaviours of workers that collectively result in worker Sb discrimination. This information fills a critical gap in the map between genotype and complex phenotype in S. invicta by restricting the search for candidate genes and molecules involved in producing this complex social trait to factors associated with the Sb element itself.