Embryo polarity in moth flies and mosquitoes relies on distinct old genes with localized transcript isoforms

Abstract

Unrelated genes establish head-to-tail polarity in embryos of different fly species, raising the question of how they evolve this function. We show that in moth flies (<i>Clogmia</i>, <i>Lutzomyia</i>), a maternal transcript isoform of <i>odd-paired (Zic)</i> is localized in the anterior egg and adopted the role of anterior determinant without essential protein change. Additionally, <i>Clogmia</i> lost maternal germ plasm, which contributes to embryo polarity in fruit flies (<i>Drosophila</i>). In culicine (<i>Culex</i>, Aedes) and anopheline mosquitoes (Anopheles), embryo polarity rests on a previously unnamed zinc finger gene (<i>cucoid</i>), or <i>pangolin</i> (<i>dTcf</i>), respectively. These genes also localize an alternative transcript isoform at the anterior egg pole. Basal-branching crane flies (<i>Nephrotoma</i>) also enrich maternal <i>pangolin</i> transcript at the anterior egg pole, suggesting that <i>pangolin</i> functioned as ancestral axis determinant in flies. In conclusion, flies evolved an unexpected diversity of anterior determinants, and alternative transcript isoforms with distinct expression can adopt fundamentally distinct developmental roles.