Simple inheritance, complex regulation: supergene-mediated fire ant
queen polymorphism
Abstract
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.