Two insulin receptors determine alternative wing morphs in planthoppers

Abstract

Wing polyphenism is an evolutionarily successful feature found in a wide range of insects. 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. Studies on aphids, crickets and planthoppers have revealed that alternative wing morphs develop in response to various environmental cues, 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. 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.

Caste development and evolution in ants: it's all about size

“…IIS may also be responsible for the reduction in eye size and wing size observed in small D. melanogaster individuals (Tang et al, 2011). More extreme variation in tissue growth has been observed in other insects, where it is associated with IIS, but also JH, ecdysone and even the hedgehog signaling pathway (Lobbia et al, 2003;Emlen et al, 2012;Gotoh et al, 2014;Niitsu et al, 2014;Kijimoto and Moczek, 2016;Xu et al, 2015; see also the excellent discussion in Zinna et al, 2016). Any or all of these factors (and others yet to be discovered) are candidate caste differentiation factors in ants.…”

“…Here, we attempt to unify the literature on ant caste development and evolution with a single theoretical framework, drawing on recent advances in evolutionary developmental biology (Carroll et al, 2001;West-Eberhard, 2003;Hartfelder and Emlen, 2012;Bopp et al, 2014;Wagner, 2014;Londe et al, 2015;Xu et al, 2015). We propose that ants possess a developmental spectrum of phenotypes, with increasing body size associated with increasingly queen-like traits (Fig.…”

Insulin receptors and wing dimorphism in rice planthoppers

“…NlInR1 and NlInR2 closely resemble each other as well as their Drosophila counterpart with respect to amino acid identity and domain architecture [50]. Surprisingly, NlInR1 and NlInR2 play fully opposite roles in wing-morph determination in the BPH.…”

“…These breakthrough findings suggest that the BPH employs the same suit of genes to generate different wing morphs in different environments by alternating their expressional levels. Further, functional studies on insulin receptors from additional two planthopper species, L. striatellus and S. furcifera, indicated that the planthopper family might share a common regulatory mechanism underlying wing dimorphism [50]. Thus, we refer to the wing-morph plasticity in planthoppers as wing polyphenism instead of wing polymorphism, as alternative wing morphs are caused by redeployment of the existing developmental pathways, but are not genetically determined.…”

“…Although the data are limited, we speculate that more insects encoding two or more InRs will be revealed as more genomic sequences become available. By examining the structural difference between NlInR1 and NlInR2 in the BPH, we found that the second InR (NlInR2) lacks four cysteine residues adjacent to the amino-terminal part of the furin-like cysteine-rich region (Fu) domain [50] that plays an important functional role in the interaction of the receptor with insulin [51,52]. Especially, only one cysteine at position 550 (C 550 ), numbered after the Drosophila counterpart, is found within the amino-terminal portion of the Fu domain in the NlInR2, whereas concatenate residues of two cysteines (C 549 C 550 ) are present in the corresponding position in NlInR1 (figure 2).…”