Brain Gene Expression of Foraging Behavior and Social Environment in Ceratina calcarata

Abstract

Rudimentary social systems have the potential to both advance our understanding of how complex sociality may have evolved and our understanding of how changes in social environment may influence gene expression and cooperation. Recently, studies of primitively social Hymenoptera have greatly expanded empirical evidence for the role of social environment in shaping behavior and gene expression. Here, we compare brain gene expression profiles of foragers across social contexts in the small carpenter bee, Ceratina calcarata. We conducted experimental manipulations of field colonies to examine gene expression profiles among social contexts including foraging mothers, regular daughters, and worker-like dwarf eldest daughters in the presence and absence of mother. Our analysis found significant differences in gene expression associated with female age, reproductive status, and social environment, including circadian clock gene dyw, hexamerin, and genes involved in the regulation of juvenile hormone and chemical communication. We also found that candidate genes differentially expressed in our study were also associated with division of labor, including foraging, in other primitively and advanced eusocial insects. Our results offer evidence for the role of the regulation of key developmental hormones and circadian rhythms in producing cooperative behavior in rudimentary insect societies.

Keywords: behavioral genetics; cooperation; foraging behavior; social environment; social evolution; transcriptomics.

Fig. 1.

PCA of gene expression in foraging females of each behavioral class, across the first four PCs (PC1–PC4). Values in brackets represent percentage of total variation explained by each PC. DC, control dwarf eldest daughters with mother present; DT, dwarf eldest daughters with mother removed; M, mothers; R, regular daughters.

Fig. 2.

Counts of DEGs across each female behavioral category, with associated annotated genes (italicized), followed by enriched GO terms. Full list of DEGs and GO terms is available in supplementary table S3, Supplementary Material online. Illustration by Jesse Huisken.

Fig. 3.

Candidate DEGs with annotations for social environment, dwarf eldest daughters with mother present/absent, and for reproductive status, reproductive (regular daughters and mothers) and nonreproductive (dwarf eldest daughters). Full list of DEGs found in supplementary table S1, Supplementary Material online.

Fig. 4.

Heat map of RRHO visualizing correlations between gene expression profiles of C. calcarata reproductive (regular daughters) and nonreproductive (dwarf eldest daughters), on the x-axis, compared with reproductive and nonreproductive phenotypes in three species, on the y-axis. Scale represents relative scale of Log₁₀ transformed values from RRHO analysis.