Abstract
In holometabolous insects, the larval, pupal, and adult stages are determined by three metamorphic genes: chinmo, broad, and E93, respectively. A temporal endocrine landscape, involving ecdysteroids, juvenile hormone (JH), and myoglianin, acts on these genes to move insects through their life history. Chinmo is anti-metamorphic and suppresses the expression of broad and E93. The JH target gene Krüppel-homolog 1 (Kr-h1) also suppresses metamorphosis, but the need for JH in maintaining the larva varies. Early larval molts are JH-independent, but later ones use JH (via Kr-h1) to maintain larval molting and suppress E93 expression until larvae cross a size threshold for metamorphosis. Myoglianin and/or ecdysteroids cause broad expression, and the decline in JH can stimulate E93. Based on whether JH is needed to maintain the larva, either E93 (Tribolium) or broad (Drosophila) serves as the entry to metamorphosis. Inhibitory interactions between broad and E93, and a return of JH in the prepupa, ensure that Broad and pupa formation occur before E93 and adult differentiation. In hemimetabolous insects, Chinmo and JH, via Kr-h1, maintain the nymphal stage and suppress E93 and adult differentiation. Broad is co-expressed with chinmo, and they collaborate to direct nymphal growth, especially of the wing pads. Chinmo supports isomorphic growth, while Broad supports positive allometric growth. The evolution of mutual inhibition between these two high-level transcription factors was a key innovation in the transition to holometaboly. It allowed imaginal primordia to rapidly expand through self-renewing growth in the larva before transitioning to morphogenetic growth to form the pupa.
