Genomic Features Underlying the Origin of Sociality and the Diversification of Caste Systems in Termites

Termite colonies consist of distinct castes whose developmental pathways fall into 2 types and vary among lineages. Understanding caste evolution and the diversification of developmental mechanisms is central to termite evolutionary biology. A recent hypothesis suggests that functional diversification via gene duplication contributed to termite eusocial evolution. However, genome-wide analysis is currently limited to a single species, Reticulitermes speratus, preventing comparisons of differences in gene duplication patterns and caste-specific gene expression among representatives of the 2 alternative developmental pathway types. We performed whole-genome sequencing and RNA-seq across castes from the Japanese population of Zootermopsis nevadensis. Duplicated genes exhibited more caste-specific expression than single-copy genes, supporting their role in functional diversification. Comparison with the closest termite relative, the noneusocial woodroach Cryptocercus punctulatus, identified 58 gene groups specifically duplicated in termites. Among the 147 Z. nevadensis genes in these groups, 88 GO biological process terms, including those related to genitalia morphogenesis, were significantly enriched. Moreover, some gene families duplicated in R. speratus and Z. nevadensis included paralogs highly expressed in termite-specific soldiers. Transcriptome comparisons between caste and sex of Z. nevandensis and R. speratus revealed notable differences reflecting their developmental pathways. In particular, Doublesex expression did not differ among castes in Z. nevadensis, but was significantly higher in male reproductives than in male sterile castes in R. speratus. Our findings support the hypothesis that gene duplications, particularly in reproduction and development, contributed to termite eusociality and suggest that lineage-specific changes in Doublesex-related expression may underlie the diversification of caste developmental pathways.