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Evolution of complete metamorphosis through temporal shifts in Chronologically inappropriate morphogenesis (Chinmo) and Broad

Hana Nagata, Yuichiro Suzuki

2025Development8 citationsDOIOpen Access PDF

Abstract

The origin of complete metamorphosis in insects is one of the major unresolved mysteries of insect evolution. The proposed juvenile stage regulator chronologically inappropriate morphogenesis (chinmo) may provide some insights into the evolution of metamorphosis. Here, we examined the function of Chinmo in the hemimetabolous milkweed bug Oncopeltus fasciatus. chinmo and br were co-expressed throughout the nymphal stage in this species. chinmo knockdown in these insects resulted in an enhanced rate of wing pad growth and cuticular morphogenesis, and the appearance of characteristics seen in older nymphal instars, ultimately leading to precocious adult development through the upregulation of Ecdysone-induced protein 93F. The enhanced wing pad growth of chinmo knockdown nymphs could be rescued through the knockdown of br, although br expression was not altered when chinmo was knocked down. We propose that during the evolution of holometaboly, the expression and functions of chinmo and br became temporally separated to create the unique larval-specific and pupal morphologies. Furthermore, our findings demonstrate that nymphal stages can be compressed into fewer instars, supporting the notion that insect metamorphosis evolved through drastic heterochronic shifts in life history stages.

Topics & Concepts

BiologyMetamorphosisGene knockdownMorphogenesisHeterochronyInsectNymphJuvenile hormoneLarvaPupaEvolutionary biologyWingZoologyInstarJuvenileCell biologyDevelopmental stageDevelopmental biologyLongevityImaginal discRegulatorBiological evolutionAnatomyAdaptation (eye)Life historyInsect growth regulatorEcologyDownregulation and upregulationAdaptive valueNeurobiology and Insect Physiology ResearchDevelopmental Biology and Gene RegulationFossil Insects in Amber
Evolution of complete metamorphosis through temporal shifts in Chronologically inappropriate morphogenesis (Chinmo) and Broad | Litcius