To gain insights into how juvenile hormone (JH) came to regulate insect metamorphosis, we studied its function in the ametabolous firebrat, Thermobia domestica. Highest levels of JH occur during late embryogenesis, with only low levels thereafter. Loss-of-function and gain-of-function experiments show that JH acts on embryonic tissues to suppress morphogenesis and cell determination and to promote their terminal differentiation. Similar embryonic actions of JH on hemimetabolous insects with short germ band embryos indicate that JH's embryonic role preceded its derived function as the postembryonic regulator of metamorphosis. The postembryonic expansion of JH function likely followed the evolution of flight. Archaic flying insects were considered to lack metamorphosis because tiny, movable wings were evident on the thoraces of young juveniles and their positive allometric growth eventually allowed them to support flight in late juveniles. Like in Thermobia, we assume that these juveniles lacked JH. However, a postembryonic reappearance of JH during wing morphogenesis in the young juvenile likely redirected wing development to make a wing pad rather than a wing. Maintenance of JH then allowed wing pad growth and its disappearance in the mature juvenile then allowed wing differentiation. Subsequent modification of JH action for hemi- and holometabolous lifestyles are discussed.

Department of Biological Sciences and BSI Florida International University Miami United States

Department of Biology University of Washington Seattle United States

Department of Parasitology Faculty of Science University of South Bohemia Ceské Budejovice Czech Republic

Department of Zoology Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic

Friday Harbor Laboratories University of Washington Friday Harbor United States

Institute of Entomology Biology Centre of the Czech Academy of Sciences Ceske Budejovice Czech Republic

Institute of Parasitology Biology Centre of the Czech Academy of Sciences Ceske Budejovice Czech Republic

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bioRxiv. 2024 Jan 18:2023.10.06.561279. doi: 10.1101/2023.10.06.561279. PubMed

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