Social caste switching triggers emergence of novel cellular identities in Zootermopsis termites

A hallmark of eusocial insects is the specialisation of individuals into castes that share the same genome but present distinct phenotypes. Caste switching can affect gene expression1,2, but can it give rise to entirely new cell types? Here, we generated single-cell transcriptomic atlases of a king, a queen, a soldier, and six workers of the termite Zootermopsis nevadensis to understand whether caste differentiation is accompanied by the emergence of novel cellular identities. Out of 24 annotated termite cell types, 18 of which mirrored homologous Drosophila cell types, one was unique for king, one was almost entirely restricted to the queen, and none were exclusive to nonreproductives. Instead, nonreproductive termites possessed more muscle and neuronal cells and less fat cells than reproductives. Caste-linked transcriptional signatures were detected in most cell types, including rare genes expressed with dual specificity for both cell type and caste. Despite the emergence of new cell types in reproductives, expression of hormones, immune genes, carbohydrate-active enzymes3, and rapidly adapting genes4 were only weakly altered by caste. These findings show that cellular differentiation can be induced anew in adult organisms without dysregulating their key physiologic pathways.