Letter | Published:

Two insulin receptors determine alternative wing morphs in planthoppers

Nature volume 519, pages 464467 (26 March 2015) | Download Citation


Wing polyphenism is an evolutionarily successful feature found in a wide range of insects1. Long-winged morphs can fly, which allows them to escape adverse habitats and track changing resources, whereas short-winged morphs are flightless, but usually possess higher fecundity than the winged morphs1,2,3. Studies on aphids, crickets and planthoppers have revealed that alternative wing morphs develop in response to various environmental cues1,2,4,5,6,7,8, and that the response to these cues may be mediated by developmental hormones, although research in this area has yielded equivocal and conflicting results about exactly which hormones are involved4,8,9,10. As it stands, the molecular mechanism underlying wing morph determination in insects has remained elusive. Here we show that two insulin receptors in the migratory brown planthopper Nilaparvata lugens, InR1 and InR2, have opposing roles in controlling long wing versus short wing development by regulating the activity of the forkhead transcription factor Foxo. InR1, acting via the phosphatidylinositol-3-OH kinase (PI(3)K)–protein kinase B (Akt) signalling cascade, leads to the long-winged morph if active and the short-winged morph if inactive. InR2, by contrast, functions as a negative regulator of the InR1–PI(3)K–Akt pathway: suppression of InR2 results in development of the long-winged morph. The brain-secreted ligand Ilp3 triggers development of long-winged morphs. Our findings provide the first evidence of a molecular basis for the regulation of wing polyphenism in insects, and they are also the first demonstration—to our knowledge—of binary control over alternative developmental outcomes, and thus deepen our understanding of the development and evolution of phenotypic plasticity.

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Data deposits

The cDNA sequences of NlInR1 and NlInR2 have been deposited in GenBank under accession numbers KF974333 and KF974334, respectively. Gene sequences used for dsRNA synthesis have been deposited in GenBank under the following accession numbers: KF974335 (NlChico), KF974336 (NlLnk), KF974337 (NlAkt), KF974338 (NlPten), KF974339 (NlFoxo), KF974340KF974343 (NlIlp1–4), KF974348 (NlErk), KF974349 (NlRaf), KF974350 (NlTor), KM099280 (NlRaptor), KM099281 (NlRheb), KF974344 (SfInR1), KF974345 (SfInR2), KF974346 (LsInR1) and KF974347 (LsInR2).


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We thank R.-Z. Zhang for help with BPH imaging (Fig. 1a). This work was supported by the National Basic Research Program of China (973 Program, no. 2010CB126205) and by the National Science Foundation of China (no. 31201509 and no. 31471765).

Author information

Author notes

    • Hai-Jun Xu
    •  & Jian Xue

    These authors contributed equally to this work.


  1. State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China

    • Hai-Jun Xu
    • , Jian Xue
    • , Bo Lu
    • , Xue-Chao Zhang
    • , Ji-Chong Zhuo
    • , Shu-Fang He
    • , Xiao-Fang Ma
    • , Ya-Qin Jiang
    • , Hai-Wei Fan
    • , Ji-Yu Xu
    • , Yu-Xuan Ye
    • , Peng-Lu Pan
    • , Qiao Li
    • , Yan-Yuan Bao
    •  & Chuan-Xi Zhang
  2. Department of Biology, Duke University, Durham, North Carolina 27708, USA

    • H. Frederik Nijhout


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H.-J.X. conceived and designed the study, wrote the paper, helped perform experiments and analysed the data. J.X. performed most experiments and helped with data analysis. B.L., Y.-Q.J., Q.L., S.-F.H. and J.-Y.X. helped perform experiments and antibody preparation. X.-C.Z. and J.-C.Z. performed gene cloning and immunoprecipitation. X.-F.M. performed RACE experiments. H.-W.F., Y.-X.Y. and P.-L.P. performed qRT–PCR. Y.-Y.B. and H.F.N. discussed data and revised the manuscript. C.-X.Z. organized and directed the project.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Hai-Jun Xu or Chuan-Xi Zhang.

Extended data

Supplementary information

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  1. 1.

    Supplementary information

    This file contains Supplementary notes 1-9 and Supplementary References.

Excel files

  1. 1.

    Supplementary Data

    This file contains Supplementary Table 1 which shows the sex ratio of BPHs following dsNlInRs treatments.

  2. 2.

    Supplementary Data

    This file contains Supplementary Table 2, a list of the main primers used in this study.


  1. 1.

    An immunofluorescence assay of NlILP3 in brains of 5th-instar nymphs

    The stained nerve cords (red) were crossed over a short distance from the medial neurosecretory cells to extend backwards in an arc through the brain. The cell nucleus is stained with DAPI (blue).

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