Worker-to-ergatoid differentiation is associated with reproductive maturation and DNA repair-related transcriptional remodeling in Reticulitermes chinensis.

Termite reproductives provide a useful system for examining molecular changes associated with reproductive differentiation because secondary reproductives can arise from worker-like individuals. Here, we compared workers and worker-derived ergatoids of Reticulitermes chinensis to characterize transcriptional changes associated with the acquisition of reproductive status. Histological observations revealed developed gonads containing vitellogenic oocytes in female 10-day post-differentiation ergatoids and spermatids and spermatozoa in male 10-day post-differentiation ergatoids. Transcriptome sequencing, targeted gene set enrichment analysis, weighted gene co-expression network analysis, and RT-qPCR revealed caste-associated changes in the expression of genes annotated to DNA repair-related pathways. Gene sets associated with homologous recombination, p53/checkpoint signaling and mismatch repair were significantly positively enriched toward the ergatoid-associated end of the ranked gene list, whereas the Fanconi anemia-related repair gene set showed a positive but non-significant enrichment trend. Several mismatch repair genes, including MSH2, MSH6, and MLH1, showed higher transcript abundance in ergatoids, and MLH1 retained conserved sequence and domain features across representative insects. These findings indicate that worker-to-ergatoid differentiation is associated with reproductive maturation and coordinated transcriptional remodeling of DNA repair-related genes. This study identifies candidate genes and pathways for future functional investigations of genome-maintenance-related processes during reproductive differentiation in termites.