Regulation of metamorphosis in neopteran insects is conserved in the paleopteran Cloeon dipterum (Ephemeroptera)

Abstract

Significance Mayflies are the only extant insects that molt after having formed wings, in a stage called subimago. Numerous authors have wondered whether this stage is a nymph, an adult, or a kind of intermediate. Another question is why mayflies have a subimago stage, when molting a wing is risky. Working with Cloeon dipterum , we found that metamorphosis is regulated as in neopteran insects and that it is determined prior to the formation of the subimago. Thus, it should be considered an instar of the adult stage. We also found that the forelegs grow dramatically between the last nymphal instar, the subimago, and the adult. That necessary growth may help to explain the functional sense of the subimago.

Mayfly metamorphosis: Adult winged insects that molt

“…Accordingly, Kamsoi et al (2) find that, unlike the situation in the cockroach, in the final nymphal stage of C. dipterum, E93 is expressed at only a low level (much less than seen in the adult). Perhaps this lower E93 titer is enough to promote the formation of new adultiform cuticular structures in the subimago but is too low to cause PG degeneration.…”

“…1). A paper in PNAS by Kamsoi et al (2) now presents a molecular analysis of the hormonal and cellular control of metamorphosis in a model ephemeropteran species, Cloeon dipterum , casting fresh light on the evolutionary significance of the mayfly subimaginal stage.…”

“…The paper by Kamsoi et al (2) unequivocally shows that the molt of the last nymphal stage of C. dipterum to the subimago makes use of the same hormones, receptors, and cellular signals of the MEKRE93 pathway (5) that regulate metamorphosis in all other insects. Specifically, the two successive adult molts of C. dipterum are triggered by successive pulses of the molt-initiating hormone ecdysone, a steroid secreted by the prothoracic glands (PG); the first pulse is at the end of the final nymphal instar, while the next occurs immediately on molting to subimago.…”

Kr-h1, a Cornerstone Gene in Insect Life History

“…Subsequently, Kr-h1 has been cloned in numerous insects from the holometabolan species Apis mellifera ( Grozinger et al, 2003 ), Tribolium castaneum ( Minakuchi et al, 2009 ), Aedes aegypti ( Zhu et al, 2010 ), Bombyx mori ( Kayukawa et al, 2012 ) , Helicoverpa armigera ( Zhang W.-N. et al, 2018 ), Bactrocera dorsalis ( Yue et al, 2018 ), Sitodiplosis mosellana ( Cheng et al, 2020 ), Chilo suppressalis ( Tang et al, 2020 ), Colaphellus bowringi ( Guo et al, 2021 ), and Harmoniaaxyridis ( Han et al, 2022 ) to the hemimetabolous species Blattella germanica ( Lozano and Belles, 2011 ), Pyrrhocoris apterus ( Konopova et al, 2011 ), Rhodnius prolixus ( Konopova et al, 2011 ), Locusta migratoria ( Song et al, 2014 ), Nilaparvata lugens ( Li et al, 2018 )and Sogatella furcifera ( Hu et al, 2020 ). More recently, Kr-h1 has also been characterized in two most-ancestral insect orders, the Ephemeroptera Cloeon dipterum ( Kamsoi et al, 2021 ) and the Odonata Ischnura senegalensis and Pseudothemis zonata (Okude et al, 2022), which belong to paleopterans. Alignments of the full protein sequences of the orthologs reveal that the eight zinc-finger DNA binding domains are remarkably well conserved among insect orders, as are two additional regions (LPL/PRKR and RXXSVIXXA) at the extreme C-terminus which are proved to be involved in the transcriptional inhibitory activity of Kr-h1 ( Kayukawa et al, 2012 ; Kayukawa et al, 2016 ; Li et al, 2018 ; Cheng et al, 2020 ).…”

Kr-h1, a Cornerstone Gene in Insect Life History

“…Subsequently, Kr-h1 has been cloned in numerous insects from the holometabolan species Apis mellifera [ [17] to the hemimetabolous species Blattella germanica [18], Pyrrhocoris apterus [19], Rhodnius prolixus [19], Locusta migratoria [20], Nilaparvata lugens [21] and Sogatella furcifera [22]. More recently, Kr-h1 has also been characterized in two most-ancestral insect orders, the Ephemeroptera Cloeon dipterum [23] and the Odonata Ischnura senegalensis and Pseudothemis zonata (Okude et al, 2022),which belong to paleopterans. Alignments of the full protein sequences of the orthologs reveal that the eight zincfinger DNA binding domains are remarkably well conserved among insect orders, as are two additional regions (LPL/PRKR and RXXSVIXXA) at the extreme C-terminus which are proved to be involved in the transcriptional inhibitory activity of Kr-h1 [11,14,21,24].…”