Complex patterns of differential expression in candidate master regulatory genes for social behavior in honey bees

Division of labor (DOL) in the social insects is one of nature’s most derived examples of phenotypic plasticity. Here, we explore the regulatory genomics of DOL in honey bees using RNA-Seq between nurses and foragers for eight tissues. We begin to test the hypothesis that caste-specific gene expression may be controlled in a manner analogous to how sex-specific gene expression is controlled. Specifically, we look for candidate master caste regulators that could play a role in controlling caste-specific gene expression analogous to the role played by double sex in sex-specific gene expression. We make significant first steps towards testing this hypothesis by showing that only a small number of regulatory genes show widespread differential expression across many tissues and are thus candidates for genes that could coordinate widespread patterns of gene expression in response to endocrine signals responsive to social needs. Two strong candidates are kruppel homolog-1 and double sex. Double sex, in particular, has previously been associated with sex linked phenotypic plasticity in other insects and is a promising candidate for future work. In addition to testing this primary hypothesis, we also show that the control of DOL has a complex genetic basis such that the same regulatory genes are used repeatedly in different tissues at the same caste transition in an independent manner. We further show that most regulatory genes only show differential expression in a single tissue. Overall, this study suggests candidate genes for the key regulators of social behavior in honey bees.