Deciphering the evolution of sex determination across the termite tree of life using high-quality genome assemblies

Most termites exhibit a unique sex-determining system, featuring multiple X and Y chromosomes that fuse into large complexes during male meiosis. The evolutionary origins of such complexes remain largely unknown. Using the genomes of 45 termites and two cockroaches, we investigated the evolution of sex determination systems in an entire insect lineage. We found that termite sex chromosomes are largely undifferentiated, likely reflecting extensive ongoing recombination. Evolving from the X0 system of cockroaches, most early-diverging termites exhibit a Y chromosome bearing the sex-determining gene doublesex, whereas doublesex is autosomal in most other termites. In contrast, other species exhibit multiple sex chromosomes that have undergone frequent turnover, except for Termitidae, which harbor conserved sex chromosomes. Our findings reveal important reworkings of the ancestral transformer-doublesex pathway in termites and suggest a potential role of doublesex in the formation of meiotic chromosomal complexes and caste differentiation.