The fire ant Solenopsis invicta exists in two alternate social forms: monogyne nests contain a single reproductive queen and polygyne nests contain multiple reproductive queens. This colony-level social polymorphism corresponds with individual differences in queen physiology, queen dispersal patterns, and worker discrimination behaviors, all evidently regulated by an inversion-based supergene that spans more than 13Mb of a “social chromosome,” contains over 400 protein-coding genes, and rarely undergoes recombination. The specific mechanisms by which this supergene influences expression of the many distinctive features that characterize the alternate forms remain almost wholly unknown. To advance our understanding of these mechanisms, we explore effects of social chromosome genotype and natal colony social form on gene expression in virgin queens sampled as they embarked on nuptial flights, using RNA-sequencing of two important tissues. We observe relatively minor effects of natal social form, that is, of the social/developmental environment, on gene expression profiles, but substantial effects of genotype, including i) supergene-associated gene upregulation, ii) allele-specific expression, and iii) pronounced extra-supergene trans-regulatory effects. These findings, along with observed spatial variation in differential and allele-specific expression within the supergene region, highlight the complex gene regulatory landscape that emerged following evolutionary divergence of the inversion-mediated Sb haplotype from its homolog that largely retained the ancestral gene order. The distinctive social chromosome-linked gene expression trajectories we document at the onset of a queen’s reproductive life expand the known record of relevant molecular correlates of a complex social polymorphism and point to putative genetic underpinnings of the alternate social syndromes.
