Evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termites

<jats:title>Abstract</jats:title><jats:p>The sex determination gene <jats:italic>doublesex</jats:italic> (<jats:italic>dsx</jats:italic>) encodes a transcription factor with two domains, oligomerization domain 1 (OD1) and OD2, and is present throughout insects. Sex-specific Dsx splicing isoforms regulate the transcription of target genes and trigger sex differentiation in all Holometabola examined to date. However, in some hemimetabolous insects, <jats:italic>dsx</jats:italic> is not spliced sexually and its sequence is less conserved. Here, to elucidate evolutionary changes in <jats:italic>dsx</jats:italic> in domain organisation and regulation in termites, we searched genome and/or transcriptome databases for the <jats:italic>dsx</jats:italic> OD1 and OD2 in seven termite species and their sister group (<jats:italic>Cryptocercus</jats:italic> woodroaches). Molecular phylogenetic and synteny analyses identified OD1 sequences of termites and <jats:italic>C</jats:italic>. <jats:italic>punctulatus</jats:italic> that clustered with <jats:italic>dsx</jats:italic> of Holometabola and regarded them as <jats:italic>dsx</jats:italic> orthologues. The <jats:italic>Cryptocercus dsx</jats:italic> orthologue containing OD2 was spliced sexually, as previously shown in other insects. However, OD2 was not found in all termite <jats:italic>dsx</jats:italic> orthologues. These orthologues were encoded by a single exon in three termites for which genome information is available; they were not alternatively spliced but transcribed in a male-specific manner in two examined species. Evolution of <jats:italic>dsx</jats:italic> regulation from sex-specific splicing to male-specific transcription may have occurred at an early stage of social evolution in termites.</jats:p>