The pupal specifier broad directs progressive morphogenesis in a direct-developing insect
Open accessAbstract
A key regulatory gene in metamorphosing (holometabolous) insect life histories is the transcription factor broad ( br ), which specifies pupal development. To determine the role of br in a direct-developing (hemimetabolous) insect that lacks a pupal stage, we cloned br from the milkweed bug, Oncopeltus fasciatus ( Of’br ). We find that, unlike metamorphosing insects, in which br expression is restricted to the larval–pupal transition, Of’br mRNA is expressed during embryonic development and is maintained at each nymphal molt but then disappears at the molt to the adult. Induction of a supernumerary nymphal stage with a juvenile hormone (JH) mimic prevented the disappearance of br mRNA. In contrast, induction of a precocious adult molt by application of precocene II to third-stage nymphs caused a loss of br mRNA at the precocious adult molt. Thus, JH is necessary to maintain br expression during the nymphal stages. Injection of Of’br dsRNA into either early third- or fourth-stage nymphs caused a repetition of stage-specific pigmentation patterns and prevented the normal anisometric growth of the wing pads without affecting isometric growth or molting. Therefore, br is necessary for the mutable (heteromorphic) changes that occur during hemimetabolous development. Our results suggest that metamorphosis in insects arose as expression of br , which conveys competence for change, became restricted to one postembryonic instar. After this shift in br expression, the progressive changes that occur within the nymphal series in basal insects became compressed to the one short period of morphogenesis seen in the larva-to-pupa transition of holometabolous insects.
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In hemimetabolous insects, br expression occurs at each nymphal moult, except between the last nymphal stage and the adult.
“In hemimetabolous insects, br expression occurs at each nymphal moult, except between the last nymphal stage and the adult (Erezyilmaz et al. , 2006).”
From Why grow up? <scp>A</scp> perspective on insect strategies to avoid metamorphosis (2016) · cites this paper as Erezyilmaz et al., 2006
The Results report that br mRNA rises at nymphal molts but is absent during formation of the adult cuticle in the milkweed bug Oncopeltus fasciatus. The claim extends that finding to hemimetabolous insects generally, whereas the paper’s direct evidence is for this species. No page numbers are supplied in our copy. (LLM, conf=0.82)
Experimental — accuracy not yet measuredBroad knockdown nymphs maintain the color pattern displayed at the time of the knockdown through the remaining nymphal instars.
“Broad knockdown nymphs maintain the color pattern displayed at the time of the knockdown through the remaining nymphal instars [16,43].”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [16]
The Results and Fig. 2 caption report that early fourth-instar knockdown produced fifth-instar nymphs with fourth-instar pigmentation, and that some third-instar knockdown nymphs resembled third instars after their next molt. They do not establish that the color pattern present at knockdown persists through all remaining nymphal instars: other third-instar knockdown nymphs molted to normal fourth instars before producing altered fifth instars. Our copy provides no page numbers for these passages. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn holometabolous insects the expression of chinmo and broad is separated, with Chinmo directing the early proliferative expansion of the primordium, followed by Broad directing its morphogenesis into a pupal wing.
“The expression of these two genes is separated in the holometabolous insects, with Chinmo directing the early proliferative expansion of the primordium, followed by Broad directing its morphogenesis into a pupal wing.”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [16]
The Abstract and Discussion describe Broad expression at the larval–pupal transition and its role in morphogenesis in holometabolous insects. Our copy does not mention Chinmo or establish that Chinmo first drives proliferative expansion of a wing primordium, so it does not support the proposed sequence of the two genes. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn cockroaches and bugs, broad is expressed through the nymphal series in a temporal fashion very similar to chinmo.
“Studies in both cockroaches [21] and bugs [33,16,43] showed that broad is expressed through the nymphal series in a temporal fashion very similar to chinmo (Figure 4a)”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [16]
The Results (page not provided) show that broad mRNA is present across the milkweed bug’s nymphal stages, rises at nymphal molts, and is absent when the adult cuticle forms. This supports the bug-expression portion attributed to this source, but our copy does not compare that temporal pattern with chinmo. The cockroach finding is separately cited in the sentence. (LLM, conf=0.85)
Experimental — accuracy not yet measuredBroad knockdown nymphs differ from normal nymphs in that their wing pads grow isometrically with the rest of the body rather than showing positive allometric growth.
“They differ from normal nymphs in that their wing pads grow isometrically with the rest of the body rather than showing positive allometric growth [22,16,43].”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [16]
The Results report that Broad knockdown reduces wing-pad growth while leaving leg and antenna growth unaffected. They say wing growth becomes “more isometric,” not fully isometric: the wing-pad diagonal still grows 2.0-fold, compared with 1.5-fold for the legs and antennae. The claim overstates the degree of isometry. (LLM, conf=0.88)
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 [16]
The Results (page not provided) show that broad is critical for anisometric wing-pad growth in the milkweed bug: knocking it down reduces that growth. Neither the supplied passages nor a search of our copy for chinmo supports simultaneous expression of chinmo and broad or collaboration between them. (LLM, conf=0.89)
Experimental — accuracy not yet measuredBroad knockdown does not cause precocious metamorphosis in hemimetabolous insects.
“Broad knockdown, however, does not cause precocious meta morphosis [21,33,16,43].”
From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [16]
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- Authors
- Erezyilmaz, D. F., Riddiford, L. M., & Truman, J. W.
- Affiliations
- University of Washington (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2006-05-02
- Volume
- 103
- Issue
- 18
- Pages
- 6925-6930
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- OpenAlex
- W2092513725
- Cited by
- 122
- References
- 38
- Citations by year
- 2026: 9 · 2025: 6 · 2024: 4 · 2023: 5 · 2022: 4 · 2021: 4 · 2020: 8 · 2019: 11 · 2018: 2 · 2017: 2 · 2016: 9 · 2015: 2 · 2014: 9 · 2013: 5 · 2012: 3
- FWCI
- 3.54
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (9904959)
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM060122, GM 60122)
- 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 › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Hemiptera Insect Studies
- Keywords
- Oncopeltus fasciatus, milkweed bug, hemimetabolous development, direct development, nymphal instars, juvenile hormone, precocene II, morphogenesis, pigmentation patterns, holometabolous insects, developmental gene expression
- MeSH terms
- Animals, Juvenile Hormones, Metamorphosis, Biological, Molecular Sequence Data, Morphogenesis, Nymph, Pigmentation, RNA, Transcription Factors, Wings, Animal, Insect Proteins, Heteroptera, Drosophila Proteins
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