Double abdomen in a short-germ insect: Zygotic control of axis formation revealed in the beetle<i>Tribolium castaneum</i>

Abstract

The distinction of anterior versus posterior is a crucial first step in animal embryogenesis. In the fly <i>Drosophila</i>, this axis is established by morphogenetic gradients contributed by the mother that regulate zygotic target genes. This principle has been considered to hold true for insects in general but is fundamentally different from vertebrates, where zygotic genes and Wnt signaling are required. We investigated symmetry breaking in the beetle <i>Tribolium castaneum</i>, which among insects represents the more ancestral short-germ embryogenesis. We found that maternal <i>Tc-germ cell-less</i> is required for anterior localization of maternal <i>Tc-axin</i>, which represses Wnt signaling and promotes expression of anterior zygotic genes. Both RNAi targeting <i>Tc-germ cell-less</i> or double RNAi knocking down the zygotic genes <i>Tc-homeobrain</i> and <i>Tc-zen1</i> led to the formation of a second growth zone at the anterior, which resulted in double-abdomen phenotypes. Conversely, interfering with two posterior factors, <i>Tc-caudal</i> and Wnt, caused double-anterior phenotypes. These findings reveal that maternal and zygotic mechanisms, including Wnt signaling, are required for establishing embryo polarity and induce the segmentation clock in a short-germ insect.