Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

Abstract

The early embryo of the cockroach Blattella germanica exhibits high E93 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 E93 . 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 E93 expression data in embryo and preadult stages, finding that embryonic expression of E93 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). E93 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 Thermobia domestica , E93 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 E93 expression in the embryo of hemimetabolans facilitated the larval development and the emergence of holometaboly. Independent decreases of E93 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.

The embryonic role of juvenile hormone in the firebrat,Thermobia domestica,reveals its function before its involvement in metamorphosis

“…The ametabolous order, Zygentoma, provides the only data for an ametabolous insect, Thermobia (Fig. 2A; Fernandez-Nicolas et al ., 2023). Palaeopteran postembryonic data from the mayfly, Cloeon dipterum (Kamsoi et al, 2021).…”

“…In Thermobia, JH levels are then quite low in the juvenile (Fig. 2A; Fernandez-Nicolas et al ., 2023), indicating that JH is not needed to maintain the juvenile form. Watson (1967) showed that the appearance of scales in its J4 stage is suppressed by JH application, but we have not been able to induce premature scale formation in the J3 stage by treatment of the J1 and J2 stages with 7EP (Truman and Riddiford, unpublished).…”

“…Direct hormone measurements (Fig. 2A), and Kr-h1 transcript levels (Fernandez-Nicolas et al, 2023) indicate that JH levels are low at hatching and remain low throughout juvenile growth and into the adult. In hemimetabolous insects, by contrast, JH titer measurements or Kr-h1 expression data are available for examples of paleopteran (mayflies; Kamsoi et al, 2021), polyneopteran (including grasshoppers and cockroaches: Temin et al, 1986;Lanzrein et al, 1985;Maestro, et al, 2010) and paraneopteran orders (heteropteran, Konopová et al, 2011).…”

“…Except for a possible involvement in the appearance of scales in the fourth instar juvenile (Watson, 1967), JH appears to have little or no role in the postembryonic development of Thermobia. Using levels of Kr-h1 as a proxy for the JH titer, Kr-h1 levels are low through juvenile growth and there is no dip in Kr-h1 levels during the transition to the adult stage (Fernandez-Nicolas et al, 2023). Nor is there evidence that JH is involved in sex-specific differentiation (production of genitalia) in Thermobia.…”

Stem cell-specific ecdysone signaling regulates the development and function of aDrosophilasleep homeostat

“…The terminal selector genes regulate the expression of effector genes, and an overlap of unique effector genes endows neurons with distinct anatomical and functional properties. Ecdysone and E93 regulate various developmental processes in insects 110,119,142,146 ; it will be intriguing to investigate whether E93 regulates the development of tangential input neurons in other insect species.…”