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Cited by 23Developmental Biology and Gene RegulationHymenoptera taxonomy and phylogenyNeurobiology and Insect Physiology Research

Expression of the Pupal Determinant broad during Metamorphic and Neotenic Development of the Strepsipteran Xenos vesparum Rossi

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Erezyilmaz, Deniz F., Hayward, Alex, Huang, Yan, Paps, Jordi, Acs, Zoltan, Delgado, Juan A., Collantes, Francisco, Kathirithamby, Jeyaraney·2014·PLoS ONE
DOI 10.1371/journal.pone.0093614PMC PMC3977908
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Abstract

Derived members of the endoparasitic order Strepsiptera have acquired an extreme form of sexual dimorphism whereby males undergo metamorphosis and exist as free-living adults while females remain larviform, reaching sexual maturity within their hosts. Expression of the transcription factor, broad (br) has been shown to be required for pupal development in insects in which both sexes progress through metamorphosis. A surge of br expression appears in the last larval instar, as the epidermis begins pupal development. Here we ask if br is also up-regulated in the last larval instar of male Xenos vesparum Rossi (Stylopidae), and whether such expression is lost in neotenic larviform females. We clone three isoforms of br from X. vesparum (Xv'br), and show that they share greatest similarity to the Z1, Z3 and Z4 isoforms of other insect species. By monitoring Xv'br expression throughout development, we detect elevated levels of total br expression and the Xv'Z1, Xv'Z3, and Xv'Z4 isoforms in the last larval instar of males, but not females. By focusing on Xv'br expression in individual samples, we show that the levels of Xv'BTB and Xv'Z3 in the last larval instar of males are bimodal, with some males expressing 3X greater levels of Xv'br than fourth instar femlaes. Taken together, these data suggest that neoteny (and endoparasitism) in females of Strepsiptera Stylopidia could be linked to the suppression of pupal determination. Our work identifies a difference in metamorphic gene expression that is associated with neoteny, and thus provides insights into the relationship between metamorphic and neotenic development.

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  • A lack of br up-regulation may underlie loss of complete metamorphosis via type II paedomorphosis.

    “In contrast, no evidence of elevated br expression was observed for female X. vesparum , which do not enter the pupal stage and remain larviform at maturity, suggesting that a lack of br up-regulation may underlie loss of complete metamorphosis via type II paedomorphosis (Erezyilmaz et al. , 2014).”

    From Why grow up? <scp>A</scp> perspective on insect strategies to avoid metamorphosis (2016) · cites this paper as Erezyilmaz et al., 2014

    The Results report increased br expression in fourth-instar males but not females, and the Discussion suggests that loss of a switch in br expression may underlie neoteny in X. vesparum. The paper does not identify this developmental pattern as “type II paedomorphosis,” so that specific classification is not supported by our copy. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • No evidence of elevated br expression was observed for female Xenos vesparum, which do not enter the pupal stage and remain larviform at maturity.

    “In contrast, no evidence of elevated br expression was observed for female X. vesparum , which do not enter the pupal stage and remain larviform at maturity, suggesting that a lack of br up-regulation may underlie loss of complete metamorphosis via type II paedomorphosis (Erezyilmaz et al. , 2014).”

    From Why grow up? <scp>A</scp> perspective on insect strategies to avoid metamorphosis (2016) · cites this paper as Erezyilmaz et al., 2014

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Authors
Erezyilmaz, D. F., Hayward, A., Huang, Y., Paps, J., Acs, Z., Delgado, J. A., Collantes, F., & Kathirithamby, J.
Affiliations
  • Stony Brook University (US)
  • University of Oxford (GB)
  • Universidad de Murcia (ES)
Corresponding author
Erezyilmaz, Deniz F.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2014-04-07
Volume
9
Issue
4
Pages
e93614
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0093614
PMC
PMC3977908
OpenAlex
W2074182278
Cited by
23
References
1
Citations by year
2026: 1 · 2025: 2 · 2024: 2 · 2023: 1 · 2021: 1 · 2020: 3 · 2019: 3 · 2018: 3 · 2017: 2 · 2016: 3 · 2015: 2
FWCI
0.96
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Bristol Research (University of Bristol) (publishedVersion)
  • Open Access at Essex (University of Essex) (acceptedVersion)
  • Uppsala University Publications (Uppsala University) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion)
  • Figshare (submittedVersion, cc-by)
  • Open Research Exeter (University of Exeter) (submittedVersion, cc-by)
  • Explore Bristol Research (submittedVersion)
Funders
  • Leverhulme Trust
  • Stony Brook University
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Hymenoptera taxonomy and phylogeny
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Keywords
Xenos vesparum, Strepsiptera, Stylopidae, neoteny, metamorphosis, sexual dimorphism, endoparasitism, protein isoforms, BTB domain, gene expression, last instar larva
MeSH terms
Animals, Female, Gene Expression Regulation, Insecta, Male, Metamorphosis, Biological, Pupa, Transcription Factors, Insect Proteins

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