Hemimetabolous insects elucidate the origin of sexual development via alternative splicing

Abstract

Insects are the only known animals in which sexual differentiation is controlled by sex-specific splicing. The <i>doublesex</i> transcription factor produces distinct male and female isoforms, which are both essential for sex-specific development. <i>dsx</i> splicing depends on <i>transformer</i>, which is also alternatively spliced such that functional Tra is only present in females. This pathway has evolved from an ancestral mechanism where <i>dsx</i> was independent of <i>tra</i> and expressed and required only in males. To reconstruct this transition, we examined three basal, hemimetabolous insect orders: Hemiptera, Phthiraptera, and Blattodea. We show that <i>tra</i> and <i>dsx</i> have distinct functions in these insects, reflecting different stages in the changeover from a transcription-based to a splicing-based mode of sexual differentiation. We propose that the canonical insect <i>tra-dsx</i> pathway evolved via merger between expanding <i>dsx</i> function (from males to both sexes) and narrowing <i>tra</i> function (from a general splicing factor to dedicated regulator of <i>dsx</i>).