Broad-complex functions in postembryonic development of the cockroach Blattella germanica shed new light on the evolution of insect metamorphosis
Abstract
Background Insect metamorphosis proceeds in two modes: hemimetaboly, gradual change along the life cycle; and holometaboly, abrupt change from larvae to adult mediated by a pupal stage. Both are regulated by 20-hydroxyecdysone (20E), which promotes molts, and juvenile hormone (JH), which represses adult morphogenesis. Expression of Broad-complex (BR-C) is induced by 20E and modulated by JH. In holometabolous species, like Drosophila melanogaster, BR-C expression is inhibited by JH in young larvae and enhanced in mature larvae, when JH declines and BR-C expression specifies the pupal stage. Methods Using Blattella germanica as a basal hemimetabolous model, we determined the patterns of expression of BR-C mRNAs using quantitative RT-PCR, and we studied the functions of BR-C factors using RNA interference approaches. Results We found that BR-C expression is enhanced by JH and correlates with JH hemolymph concentration. BR-C factors appear to be involved in cell division and wing pad growth, as well as wing vein patterning. Conclusions In B. germanica, expression of BR-C is enhanced by JH, and BR-C factors appear to promote wing growth to reach the right size, form and patterning, which contrast with the endocrine regulation and complex functions observed in holometabolous species. General significance Our results shed new light to the evolution from hemimetaboly to holometaboly regarding BR-C, whose regulation and functions were affected by two innovations: 1) a shift in JH action on BR-C expression during young stages, from stimulatory to inhibitory, and 2) an expansion of functions, from regulating wing development, to determining pupal morphogenesis.
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Broad 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 [21]
Section 3.2 (p. 11) reports that Broad-complex-depleted Blattella germanica nymphs molted normally through subsequent nymphal stages before reaching adulthood, rather than metamorphosing precociously. This supports the claim for the cockroach studied, but not its categorical extension to hemimetabolous insects generally. (LLM, conf=0.84)
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 [21]
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The pupal specifier <i>broad</i> directs progressive morphogenesis in a direct-developing insect
Erezyilmaz, D. F., Riddiford, L. M., & Truman, J. W. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509983103 · Cited by 122 · see citing works
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Chafino, S., Giannios, P., Casanova, J., Martín, D., & Franch-Marro, X. (2023) · eLife · doi:10.7554/elife.84648 · Cited by 30 · see citing works
Erezyilmaz, D. F., Hayward, A., Huang, Y., Paps, J., Acs, Z., Delgado, J. A., Collantes, F., & Kathirithamby, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093614 · Cited by 23 · see citing works
Regulation of metamorphosis in holometabolous insects
Truman, J. W., & Riddiford, L. M. (2026) · Current Opinion in Insect Science · doi:10.1016/j.cois.2026.101508 · Cited by 6 · see citing works
- Authors
- Huang, J.-H., Lozano, J., & Belles, X.
- Affiliations
- Universitat Pompeu Fabra (ES)
- ORCID
- Huang, Jia-Hsin
- Venue
- Biochimica et Biophysica Acta (BBA) - General Subjects
- Publisher
- Elsevier BV
- Published
- 2013-01
- Volume
- 1830
- Issue
- 1
- Pages
- 2178-2187
- ISSN
- 0304-4165 (ISSN-L)
- OpenAlex
- W2116476141
- Cited by
- 101
- References
- 1
- Citations by year
- 2026: 8 · 2025: 7 · 2024: 10 · 2023: 1 · 2022: 4 · 2021: 8 · 2020: 13 · 2019: 13 · 2018: 4 · 2017: 8 · 2016: 8 · 2015: 7 · 2014: 7 · 2013: 3
- FWCI
- 2.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biochimica et Biophysica Acta (BBA) - General Subjects (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Explore Bristol Research (submittedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Funders
- Spanish MICINN (CGL2008-03517/BOS)
- CSIC (2010TW0019)
- National Research Council (Taiwan)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Insect and Arachnid Ecology and Behavior
- Keywords
- Broad-Complex, Blattella germanica, cockroaches, insect metamorphosis, hemimetabolism, holometabolism, juvenile hormone, 20-hydroxyecdysone, postembryonic development, wing development, gene expression regulation
- MeSH terms
- Animals, Ecdysterone, Biological Evolution, Hemolymph, Juvenile Hormones, Larva, Metamorphosis, Biological, Blattellidae
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