The brain atlas of a subsocial bee reflects that of eusocial Hymenoptera

Abstract

The evolutionary transition from solitary life to group-living in a society with cooperative brood care, reproductive division of labor and morphological castes is associated with increased cognitive demands for task-specialization. Associated with these demands, the brains of eusocial Hymenoptera divide transcriptomic signatures associated with foraging and reproduction to different populations of cells and also show diverse astrocyte and Kenyon cell types compared with solitary non-hymenopteran insects. The neural architecture of subsocial bees, which represent evolutionary antecedent states to eusocial Hymenoptera, could then show how widely this eusocial brain is conserved across aculeate Hymenoptera. Using single-nucleus transcriptomics, we have created an atlas of neuron and glial cell types from the brain of a subsocial insect, the small carpenter bee (Ceratina calcarata). The proportion of C. calcarata neurons related to the metabolism of classes of neurotransmitters is similar to that of other insects, whereas astrocyte and Kenyon cell types show highly similar gene expression patterns to those of eusocial Hymenoptera. In the winter, the transcriptomic signature across the brain reflected diapause. When the bee was active in the summer, however, genes upregulated in neurons reflected foraging, while the gene expression signature of glia associated with reproductive functions. Like eusocial Hymenoptera, we conclude that neural components for foraging and reproduction in C. calcarata are compartmentalized to different parts of its brain. Cellular examination of the brains of other solitary and subsocial insects can show the extent of neurobiological conservation across levels of social complexity.

Keywords: brain evolution; cell type evolution; diapause; neurotransmitters; single cell; sociality.

FIGURE 1

The brain atlas of 8350 nuclei, divided into 10 clusters using Seurat that are then annotated with cell types using the relative expression of canonical markers, some of which are mentioned in Table 1. The cluster number is listed in the legend and the corresponding cell type of each cluster is indicated.

FIGURE 2

Proportion of neurons that express genes indicating the synthesis and/or release of classes of neurotransmitters estimated from the brain atlases of C. calcarata (this study), A. mellifera, M. pharaonsis, H. saltator, and D. melanogaster.

FIGURE 3

Volcano plots showing log₂ fold change difference in normalized expression on the x‐axis of 13,374 genes between the winter (W) and summer (S) samples. Significance indicated on the y‐axis by −log₁₀ adjusted p‐values using Bonferroni correction (i.e. false detection rate, FDR) for genes in the integrated brain atlas of (A) 6657 neuron cells combined from clusters 0, 1, 2, 4, 6, 7 and 9 in Figure 1; and (B) 1693 glia cells combined from clusters 3, 5 and 8 in Figure 1. Negative log₂ fold change indicates upregulation in W, whereas positive values indicate upregulation in S. Orange indicates those genes judged to be significantly differentially expressed and significantly upregulated to winter or summer with FDR <0.05 demarcated with the horizontal dashed line and log₂ fold change >0.05 or < −0.05 indicated by the vertical dashed line. Purple indicates those genes with a FDR ≥0.05, while pink indicates those genes with FDR <0.05, but log₂ fold change ≥ −0.5 and ≤0.5. The number of significantly differentially‐expressed genes that are upregulated in each phenotype is indicated.

FIGURE 4

Putative identities of subclusters of C. calcarata KCB (Figure 1—cluster 1) inferred from the transcriptional similarity calculated with MetaNeighbor of 4718 orthologs to small, medium and class II Kenyon cell types of A. mellifera , , and from the similarity of C. calcarata to α′/β′ and γ Kenyon cell types from D. melanogaster. Number in the legend indicates the number of the subcluster referred to in the text. Small = small Kenyon cells; med = medium Kenyon cells.