Indirect genetic effects describe phenotypic variation that results from
differences in the genotypic composition of social partners. Such
effects represent heritable sources of environmental variation in
eusocial organisms because individuals are typically reared by their
siblings. In the fire ant Solenopsis invicta, a social supergene
exhibits striking indirect genetic effects on worker regulation of
colony queen number, such that the genotypic composition of workers at
the supergene determines whether colonies contain a single or multiple
queens. We assessed the direct and indirect genetic effects of this
supergene on gene expression in brains and abdominal tissues from
lab-reared workers and compared these with previously published data
from field-collected pre-reproductive queens. We found that direct
genetic effects caused larger gene expression changes and were more
consistent across tissue types and castes than indirect genetic effects.
Indirect genetic effects influenced the expression of many loci but were
generally restricted to the abdominal tissues. Further, indirect genetic
effects were only detected when the genotypic composition of social
partners differed throughout the development and adult life of focal
workers, and were often only significant with relatively lenient
statistical cutoffs. Our study provides insight into direct and indirect
genetic effects of a social supergene on gene regulatory dynamics across
tissues and castes in a complex society.