Insulin receptors and wing dimorphism in rice planthoppers

Abstract

Wing polymorphism contributes significantly to the success of a wide variety of insects. However, its underlying molecular mechanism is less well understood. The migratory planthopper (BPH), Nilaparvata lugens, is one of the most extensively studied insects for wing polymorphism, due to its natural features of short- and long-winged morphs. Using the BPH as an example, we first surveyed the environmental cues that possibly influence wing developmental plasticity. Second, we explained the molecular basis by which two insulin receptors (InR1 and InR2) act as switches to determine alternative wing morphs in the BPH. This finding provides an additional layer of regulatory mechanism underlying wing polymorphism in insects in addition to juvenile hormones. Further, based on a discrete domain structure between InR1 and InR2 across insect species, we discussed the potential roles by which they might contribute to insect polymorphism. Last, we concluded with future directions of disentangling the insulin signalling pathway in the BPH, which serves as an ideal model for studying wing developmental plasticity in insects.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

Keywords: insulin receptors; phenotypic plasticity; planthoppers; wing polymorphism.

Figure 1.

Wing dimorphism of the brown planthopper Nilaparvata lugens. (Online version in colour.)

Figure 2.

Alignment of the furin-like cysteine-rich (Fu) domains of insect InRs. The insect InR contains a typical domain architecture that consists of a signal peptide (SP), two ligand-binding loops (L1 and L2), a Fu region, three fibronectin type 3 domains (Fn3), a single transmembrane (TM) and a tyrosine kinase (TyrKc). Amino acid sequences of the Fu domain are selected from nine insect species that represent orders of Anoplura, Blattodea, Coleoptera, Diptera, Hemiptera, Hymenoptera and Lepidoptera, respectively. Concatenate residues of two cysteines (C⁵⁴⁹C⁵⁵⁰) are indicated with stars. Znev: Zootermopsis nevadensis; Bger: Blattella germanica; Nlug: Nilaparvata lugens; Amel: Apis mellifera; Phco: Pediculus humanus corporis; Ldec: Leptinotarsa decemlineata; Adar: Anopheles darlingi; Dple: Danaus plexippus; Dmel: Drosophila melanogaster; Hsap: Homo sapiens. (Online version in colour.)

Figure 3.

Phylogenetic analysis of InRs from 37 insect species. A maximum-likelihood phylogenetic tree (bootstraps with 1000 replications) is created using the full-length sequences of the tyrosine kinase domains of InRs and anaplastic lymphoma kinase (Alk). The GenBank accession numbers of InRs are indicated in electronic supplementary material, table S1. The InR1 and InR2 branches are at the upper clade (shown in green and blue lines, respectively), and orders are listed on the right. Sinv: Solenopsis invicta; Veme: Vollenhovia emeryi; Waur: Wasmannia auropunctata; Acep: Atta cephalotes; Aech: Acromyrmex echinatior; Pbar: Pogonomyrmex barbatus; Lhum: Linepithema humile; Csol: Ceratosolen solmsi marchali; Nvit: Nasonia vitripennis; Aros: Athalia rosae; Hsal: Harpegnathos saltator; Fari: Fopius arisanus; Mdem: Microplitis demolitor; Mrot: Megachile rotundata; Amel: Apis mellifera; Bimp: Bombus impatiens; Bter: Bombus terrestris; Phcor: Pediculus humanus corporis; Znev: Zootermopsis nevadensis; Bger: Blattella germanica; Ldec: Leptinotarsa decemlineata; Tcas: Tribolium castaneum; Bmor: Bombyx mori; Dple: Danaus plexippus; Hmel: Heliconius melpomene; Msex: Manduca sexta; Pxyl: Plutella xylostella; Mdes: Mayetiola destructor; Aaeg: Aedes aegypti; Agam: Anopheles gambiae; Dmel: Drosophila melanogaster; Bdor: Bactrocera dorsalis; Ccap: Ceratitis capitata; Nlug: Nilaparvata lugens; Apis: Acyrthosiphon pisum; Cflo: Camponotus floridanus; Clec: Cimex lectularius; Acol: Atta colombica; Hsap: Homo sapiens. (Online version in colour.)