Localized Tissue-Specific Gene Expression and Gene Duplications are Important Sources of Social Morph Differences in a Social Bumblebee

Understanding the expression of multiple behaviorally and morphologically distinct phenotypes from a single genome represents a fundamental topic in evolutionary biology. Central to the complication of expressing phenotypes, which may differ in their optima, is the sharing of largely the same genome, which is predicted to manifest in conflict at the genomic level. This is particularly true for social insects where molecular mechanisms, such as differential gene expression, contribute to observed phenotypic differences between reproductive and nonreproductive morphs. In comparison, other mechanisms, such as tissue-specific expression and gene duplications, have been posited as contributing to social morph differences yet formal investigations are limited. Here, using a combination of transcriptomics for multiple tissues and comparative genomics, we show that in a social bumblebee, the strongest differences in gene expression are found in reproductive tissues, such as the spermatheca, an organ previously believed as vestigial in workers but recently shown as functional. In comparison, we find modest expression differences in genes between queens and workers for the brain, fat body, and ovary, which are traditionally investigated in social evolution. Interestingly, morph-biased genes in these three tissues display higher tissue-specificity suggesting that while social morphs may express a shared core transcriptome, localized expression profiles may contribute to phenotypic differences. We also find evidence of differential usage of duplicated genes by queens and workers, highlighting structural variants as a contributing factor to morph differences. Collectively, our findings highlight how social insects can utilize tissue-specific gene regulation and structural variants to contribute to phenotypic differences.