Journal Article

Two insulin receptors determine alternative wing morphs in planthoppers

Fan, Hai-Wei, Ma, Xiao-Fang, Jiang, Ya-Qin, Ye, Yu-Xuan, Zhang, Xue-Chao, Xue, Jian, Xu, Hai-Jun, Li, Qiao, Zhang, Chuan-Xi, He, Shu-Fang, Bao, Yan-Yuan, Xu, Ji-Yu, Zhuo, Ji-Chong, Pan, Peng-Lu, Nijhout, H. Frederik, Lu, Bo

2015

Overview

Some insects have alternative wing morphs, one that is long-winged and changes habitat to follow resources, and one that is short-winged and flightless but has high fertility; here, the molecular details of this switch are revealed, with opposite effects of two insulin receptors controlling the development of different wing morphs in the planthopper. Insect double identity is insulin-linked Some types of insect can exist in two forms, both as long-winged morphs that can move from habitat to habitat to follow resources, and as short-winged flightless morphs with high fertility, but the molecular details of this switch have remained unclear. One species that leads this double life is the migratory brown planthopper Nilaparvata lugens , a serious pest in rice-growing regions of Asia. Chuan-Xi Zhang and colleagues show that long-wing versus short-wing development in N. lugens is controlled through the opposing effects of two insulin receptors, InR1 and InR2, on the activity of the forkhead transcription factor Foxo. Wing polyphenism is an evolutionarily successful feature found in a wide range of insects 1 . 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 morphs 1 , 2 , 3 . Studies on aphids, crickets and planthoppers have revealed that alternative wing morphs develop in response to various environmental cues 1 , 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 involved 4 , 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.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 13 / 13/51 / 14 / 14/19 / 38 / 38/32 / 38/89 / 631/181/2806 / 96 / 96/95 / Analysis / Animals / Environmental aspects / Fecundity / Female / Forkhead Transcription Factors - deficiency / Forkhead Transcription Factors - metabolism / Genetic regulation / Genotype & phenotype / Health aspects / Hemiptera - anatomy & histology / Hemiptera - enzymology / Hemiptera - genetics / Hemiptera - metabolism / Hormones / Humanities and Social Sciences / Insects / Insulin - metabolism / Insulin-like growth factors / Kinases / letter / Ligands / Male / Molecular Sequence Data / multidisciplinary / Phosphatidylinositol 3-Kinases - metabolism / Phosphorylation / Planthoppers / Polyphenism / Proto-Oncogene Proteins c-akt - metabolism / Receptor, Insulin - deficiency / Receptor, Insulin - metabolism / Science / Signal Transduction / Wings, Animal - anatomy & histology / Wings, Animal - enzymology / Wings, Animal - growth & development / Wings, Animal - metabolism