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Cited by 8Developmental Biology and Gene RegulationNeurobiology and Insect Physiology ResearchInsect and Arachnid Ecology and Behavior

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

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Nagata, Hana, Suzuki, Yuichiro·2026·Development
DOI 10.1242/dev.204998PMC PMC12848571
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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.

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  • In hemimetabolous insects, Chinmo and JH, via Kr-h1, maintain the nymphal stage and suppress E93 and adult differentiation.

    “In hemimetabolous insects, Chinmo and JH, via Kr-h1 , maintain the nymphal stage and suppress E93 and adult differentiation.”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [43]

    The Discussion section ‘Chinmo represses E93 expression during the nymphal stage’ supports that Chinmo and JH restrain E93 and adult development. But it explicitly says they regulate E93 independently: chinmo knockdown did not change Kr-h1 expression. Thus ‘via Kr-h1’ is supported for JH, not for Chinmo. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • As in Holometabola, E93 functions in hemimetabolous species to mediate the entry into metamorphosis, and its suppression results in permanent nymphs.

    “As in the Holometabola, E93 functions in these species to mediate the entry into metamorphosis, and its suppression results in permanent nymphs [65,43].”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [43]

    The Introduction identifies E93 as an adult-specifier gene in both hemimetabolous and holometabolous insects. The Results report that E93 knockdown alone produced an extra nymphal instar; the Discussion describes permanent nymphs only after E93 and chinmo were knocked down together. The claim omits that condition for the permanent-nymph outcome. Page numbers were not available in our copy. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Lack of broad results in Oncopeltus nymphs that grow without change.

    “Lack of broad results in nymphs that grow without change”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [43]

    The Results section, “br RNAi reverses the effects of chinmo knockdown on wing pad growth” (page unavailable), reports that br knockdown reduced the rate of wing maturation in Oncopeltus nymphs. It does not say the nymphs grew without morphological change; the reported outcome was adults with smaller wings. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • In the hemimetabolous bug, chinmo and broad are expressed simultaneously and collaborate to support the positive allometric growth of the wing pads.

    “In the bug, the two genes are expressed simultaneously and collaborate to support the positive allometric growth of the wing pads.”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [43]

    The Introduction and the Discussion section ‘chinmo and br are co-expressed during the nymphal stage’ support simultaneous expression in O. fasciatus nymphs. But the Discussion section ‘Chinmo regulates isometric growth and nymphal morphogenesis’ says the genes act antagonistically: Br promotes allometric wing growth, whereas Chinmo favors isometric growth. It does not support the claim that they collaborate to promote positive allometric wing-pad growth. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Precocious 'last stage' nymphs lacking both chinmo and E93 continue to molt to additional last stage nymphs.

    “In such cases, precocious 'last stage' nymphs continue to molt to additional last stage nymphs due to a lack of E93.”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [43]

    The Results section ('E93 but not br is upregulated in chinmo knockdown nymphs'; page unavailable) reports that nymphs with both chinmo and E93 knocked down molted into another nymph rather than a precocious adult. It does not establish that these were 'last stage' nymphs or that they continued through multiple additional nymphal molts. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

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Cites

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Cited by

Sorted by citations

Authors
Nagata, H., & Suzuki, Y.
Affiliations
Wellesley College (US)
Corresponding author
Suzuki, Yuichiro
ORCID
Suzuki, Yuichiro
Venue
Development
Publisher
The Company of Biologists
Published
2026-01-01
Volume
153
Issue
1
ISSN
  • 0950-1991 (ISSN-L)
  • 1477-9129
DOI
10.1242/dev.204998
PMC
PMC12848571
OpenAlex
W4416848062
Cited by
8
References
3
Citations by year
2026: 7 · 2025: 1
FWCI
2.40
Type
journal article
Language
en
Open access
Licence
Locations
  • Development (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion, cc-by)
Funders
  • National Science Foundation (IOS-2002354)
  • Wellesley College
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Insect and Arachnid Ecology and Behavior
Keywords
complete metamorphosis, holometabolism, Chinmo, Broads, Oncopeltus fasciatus, milkweed bug, hemimetabolous insects, heterochrony, nymphal instars, juvenile hormone, insect evolution
MeSH terms
Animals, Biological Evolution, Larva, Metamorphosis, Biological, Morphogenesis, Nymph, Pupa, Wings, Animal, Gene Expression Regulation, Developmental, Insect Proteins, Heteroptera, Gene Knockdown Techniques

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