By Viviane Callier
Insulin, the hormone that controls blood glucose in humans, is also produced by insects and, according to a study published in Nature, two different insulin receptors convey cues that enable some insects to predict their future environments and to develop functionally-appropriate wings.
Some larval insects have the difficult task of predicting the environment they will inhabit as adults. For example, if resources are plentiful, the migratory brown planthopper (Nilaparvata lugens) will likely grow up to be a short-winged adult with the ability to produce many offspring. However, if resources are scarce and conditions are poor, the larva will become a long-winged adult that is better able to fly away to escape adverse conditions — at a cost to its reproductive capacity.
The wing shape is not genetically determined. Instead, it is induced by environmental cues such as temperature, nutrition, or crowding, which are good predictors of resource availability. This ability to produce two alternative wing shapes, depending on environmental cues, is called a polyphenism, and some of the most common polyphenisms in insects are seasonal (summer and winter forms). But the molecular and developmental mechanism by which these larval insects predict their future environments and develop suitable wings has remained a mystery until now.
In the new Nature study, the authors show that insulin signaling — a cellular signaling pathway that regulates growth, and which is present in animals from worms and flies to humans — controls whether the planthopper will develop long or short wings. The brain responds to environmental cues by secreting insulin, which in turn activates two different insulin receptors in the wings.
“What is so elegant about this work is that it provides an unusually detailed, mechanistic understanding of the developmental-genetic processes that integrate environmental conditions into critical components of postembryonic development, allowing alternate but nevertheless fully integrated and adaptive phenotypes to emerge in the process,” said Dr. Armin Moczek, a professor of biology at Indiana University in Bloomington who was not involved in the study.
The study shows that planthoppers have two different insulin receptors. The first (InR1) activates the main insulin signaling pathway and leads to the development of long-winged adults. The second receptor (InR2) binds to and inhibits the first, leading to short-winged adults.
“Until now it was generally thought that insects had only a single functional insulin receptor,” said Dr. H. Frederik Nijhout, professor of biology at Duke University and co-author of the study. “This work shows that in planthoppers there are at least two insulin receptors that produce very different morphological effects.”
To demonstrate how insulin controls the switch in wing forms, the researchers used a tool called RNA interference (RNAi) to block the expression of insulin-receptor genes in juvenile planthoppers. By introducing molecules of RNA into the cell, the scientists were able to interfere with the expression of the insulin-receptor genes, which prevented the cells from making either the first or the second insulin receptors, and they observed the resulting adults’ wings.
Blocking the expression of the second insulin receptor produced long-winged adults. In contrast, blocking the first insulin receptor produced short-winged adults. The long-winged morph is the default adult form, but if activated, the second receptor binds to and inhibits the first, leading to short-winged adults.
To further explore how these two receptors interact, the researchers used an immunoprecipitation assay, which uses antibodies that specifically recognize the receptors. The antibodies are flagged with a marker that can easily be detected in the lab, thus enabling the scientists to see that the two receptors physically bind to each other.
“This work provides the most detailed understanding of the molecular mechanisms underlying a polyphenic trait in any animal to date,” explained Dr. Christen Mirth, insect biologist and group leader at the Instituto Gulbenkian de Ciencia in Portugal, who was not involved in the study. “Specifically, the work uncovers a previously unknown mechanism whereby the type of insulin receptor expressed directs organ development along one of two alternative pathways.”
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Viviane Callier is trained as an insect physiologist and is now a freelance science writer in Washington, DC. Find her on Twitter at @vcallier or on her website at https://vivianecallier.wordpress.com.