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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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), KF974340–KF974343 (NlIlp1–4), KF974348 (NlErk), KF974349 (NlRaf), KF974350 (NlTor), KM099280 (NlRaptor), KM099281 (NlRheb), KF974344 (SfInR1), KF974345 (SfInR2), KF974346 (LsInR1) and KF974347 (LsInR2).
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).
Extended data figures
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).