Reduction of embryonic <i>E93</i> expression as a hypothetical driver of the evolution of insect metamorphosis.

Abstract

The early embryo of the cockroach <i>Blattella germanica</i> exhibits high <i>E93</i> expression. In general, E93 triggers adult morphogenesis during postembryonic development. Here we show that E93 is also crucial in early embryogenesis in the cockroach, as a significant number of E93-depleted embryos are unable to develop the germ band under maternal RNAi treatment targeting <i>E93</i>. Moreover, transcriptomic analysis indicates that E93 depletion results in important gene expression changes in the early embryo, and many of the differentially expressed genes are involved in development. Then, using public databases, we gathered <i>E93</i> expression data in embryo and preadult stages, finding that embryonic expression of <i>E93</i> is high in hemimetabolan species (whose juveniles, or nymphs, are similar to the adult) and low in holometabolans (whose juveniles, or larvae, are different from the adult). <i>E93</i> expression is also low in Thysanoptera and in Hemiptera Sternorrhyncha, hemimetabolans with postembryonic quiescent stages, as well as in Odonata, the nymph of which is very different from the adult. In ametabolans, such as the Zygentoma <i>Thermobia domestica</i>, <i>E93</i> transcript levels are very high in the early embryo, whereas during postembryonic development they are medium and relatively constant. We propose the hypothesis that during evolution, a reduction of <i>E93</i> expression in the embryo of hemimetabolans facilitated the larval development and the emergence of holometaboly. Independent decreases of <i>E93</i> transcripts in the embryo of Odonata, Thysanoptera, and different groups of Hemiptera Sternorrhyncha would have allowed the development of modified juvenile stages adapted to specific ecophysiological conditions.