The Evolution of Insect Metamorphosis.

The evolution of insect metamorphosis is one of the most important sagas in animal history, transforming small, obscure soil arthropods into a dominant terrestrial group that has profoundly shaped the evolution of terrestrial life. The evolution of flight initiated the trajectory towards metamorphosis, favoring enhanced differences between juvenile and adult stages. The initial step modified postembryonic development, resulting in the nymph-adult differences characteristic of hemimetabolous species. The second step was to complete metamorphosis, holometaboly, and occurred by profoundly altering embryogenesis to produce a larval stage, the nymph becoming the pupa to accommodate the deferred development needed to make the adult. These changing life history patterns were intimately linked to two hormonal systems, the ecdysteroids and the juvenile hormones (JH), which function in both embryonic and postembryonic domains and control the stage-specifying genes Krüppel homolog 1 (Kr-h1), broad and E93. The ecdysteroids induce and direct molting through the ecdysone receptor (EcR), a nuclear hormone receptor with numerous targets including a conserved transcription factor network, the 'Ashburner cascade', which translates features of the ecdysteroid peak into the different phases of the molt. With the evolution of metamorphosis, ecdysteroids acquired a metamorphic function that exploited the repressor capacity of the unliganded EcR, making it a hormone-controlled gateway for the tissue development preceding metamorphosis. JH directs ecdysteroid action, controlling Kr-h1 expression which in turn regulates the other stage-specifying genes. JH appears in basal insect groups as their embryos shift from growth and patterning to differentiation. As a major portion of embryogenesis was deferred to postembryonic life with the evolution of holometaboly, JH also acquired a potent role in regulating postembryonic growth and development. Details of its involvement in broad expression and E93 suppression have been modified as life cycles became more complex and likely underlie some of the changes seen in the shift from incomplete to complete metamorphosis.