Evolutionary origin of sex differentiation system in insects

The evolution of the functionality of genes and genetic systems is a major source of animal diversity. Its best example is insect sex differentiation systems: promoting male and female differentiation (dual-functionality) or only male differentiation (single-functionality). However, the evolutionary origin of such functional diversity is largely unknown. Here, we investigate the ancestral functions ofdoublesex, a key factor of insect sex differentiation system, using the apterygote insect,Thermobia domestica, and reveal that itsdoublesexis essential for only males at the phenotypic level, but contributes to promoting female-specificvitellogeninexpression in females. This functional discordance between the phenotypic and transcription-regulatory levels inT. domesticashows a new type of functionality of animal sex differentiation systems. Then, we examine how the sex differentiation system transited from the single-functionality to the dual-functionality in phenotypes and uncover that a conserved female-specific motif ofdoublesexis detected in taxa with the dual-functionaldoublesex. It is estimated that the role of the sex differentiation system for female phenotypes may have evolved through accumulating mutations in the protein motif structures that led to the enhancement of its transcription-regulatory function.