The Evolution of Insect Metamorphosis

Abstract

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 Kru¨ppel 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 hormonecontrolled 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.

Diversity of Insect Sesquiterpenoid Regulation

“…(E) In the last nymphal stage, the JH titers fall followed by the Kr-h1 expression level. For details, please refer to main text and Truman, 2019 .…”

Transcriptome Analysis Reveals Candidate Genes During the Prepupal-pupal Transition in the Oriental Armyworm, Mythimna separata (Walker) (Lepidoptera: Noctuidae)

“…Insect metamorphism refers to a series of changes in the external form, internal structure, physiological functions, living habits, and behavioral instincts of an insect during its development from larva to adult [30]. The pupa stage, as a sign of the holometabolous insect, is a transitional morphology that develops from a larva to an adult and with the decomposition and reconstruction of larval and adult tissues and organs in this stage [31].The research on insect metamorphic development can provide effective molecular targets for methods of pest control and bene cial insect utilization.…”

Developmental loss of neurofibromin across distributed neuronal circuits drives excessive grooming in Drosophila

“…Development of the nervous system involves many important steps that are subject to plasticity, particularly during the pupal stage in Drosophila. During metamorphosis, neurons in the CNS exhibit dramatic changes, including programmed cell death, neurogenesis and proliferation, and neurite remodeling [54][55][56]. For example, connectivity between mushroom body Kenyon cells (KC) and presynaptic GABAergic neurons is dependent on pruning initiation from the post-synaptic γ KCs [57].…”

“…The requirement for intact GAP-related domain functionality suggests that Nf1-mediated Ras signaling is important for the development of normal grooming. As explored above, several critical neural developmental events occur during metamorphosis [54,55]. Ras signaling may affect these processes by acting downstream of receptor tyrosine kinases, some of which play key roles in development [58].…”