From 250 million years of repression, a wonderland of hats

By Ed Yong | May 4, 2011 1:00 pm

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Treehoppers are insects that look like they have materialised from the imagination of a drunk fantasy artist. They would look like simple cicadas, were it not for the elaborate structures on their backs, known as “helmets”. These take the form of thorns, leaves, droppings, ants, and other shapes too bizarre to describe. They are the signature feature of the treehoppers. All 3,200 or so species have them.

The helmets may be strange and unique, but they’re related to familiar body parts found on most insects: wings. French scientists Benjamin Prud’homme and Nicolas Gompel have discovered that the helmets are actually modified wings. They are the result of ancient genetic potential, repressed for 250 million years, and unlocked by this one group.

Until now, most scientists thought that the helmet is part of the treehopper’s thorax – the middle part of its body, between its head and abdomen. The thorax is made of three segments and the treehoppers supposedly evolved their helmets by expanding the first of these, known as T1. That’s not unusual – many beetles have developed dramatic horns in a similar way. But something about this explanation didn’t make sense to Gompel.

Gompel knew that the helmets were easily discarded. His friend Gérard Moraguès, a lawyer and amateur entomologist, once told him that when he tried to catch treehoppers, he often ended up holding the broken helmet while the animal escaped. “I found this very puzzling,” says Gompel. “I couldn’t understand how an insect could afford losing its thorax, so I collected some treehoppers and dissected them. It was immediately clear to me that I was looking at modified wings.”

This is a bolder claim than it sounds. There is not a single example of a living insect with wings on T1. Wings always develop from the second and third thoracic segments – T2 and T3. Gompel was effectively claiming that this group of familiar insects has a third set of “wings”. He knew that other scientists wouldn’t just take his word for it so he spent the next several years building his case.

By carefully examining the treehopper Publilia modesta, Prud’homme and Gompel showed that its helmet is connected to the thorax by a pair of flexible, elastic joints, just as its wings are. And just like wings, the helmet develops from two small buds on in the larva. As the insect grows, these buds eventually meet in the middle of its body, and fuse into a single, continuous structure.

If these physical similarities weren’t enough, Prud’homme and Gompel also found that the helmet is built using the same genetic programmes that construct the treehopper’s wings. A gene called Nubbin*, which is normally only switched on in developing wings, is also activated in the growing helmet. Two genes called Distal-less and homothorax, which control the shape of legs and wings, also set the shape of the helmet.

When insects first evolved, they could produce wings from all three of their thoracic segments. Some fossil insects did indeed have three sets of wings. But at some point in their history, they repressed the ability to grow wings from T1. A gene called Scr (sex combs reduced) is active in T1 and prevents Nubbin and other essential wing genes from switching on. Under the repressive yoke of Scr, T1 wings have been abolished from the insect dynasty for 250 million years. That is, except in treehoppers.

Prud’homme and Gompel found that Scr is still active in the T1s of treehoppers but it has somehow lost the ability to control Nubbin and stall the development of wings. It’s like a deposed dictator, whose citizens no longer respond to its orders. By ignoring Scr, the treehoppers’ ancestors managed to unlock an evolutionary potential that had been lying dormant for millions of years.

This brings us back to a running theme in evolution – animals seldom need new genetic material to produce big changes and new body parts. Instead, they can redeploy existing genes in different ways or, in the case of the treehoppers, unlock programs that had been previously silenced.

But why did the treehoppers evolve their bizarre headgear in the first place? “We’re entering the wild guess area here,” says Gompel. He reckons that the early helmets had no role whatsoever. Rather, the important thing is that they didn’t cause the insects any harm. If mutant insects developed a third set of wings, they might die off quickly because the wings might mess with their ability to fly – they would be ‘counter-selected’. “Now if these wings are not real wings, if they are some kind of stubs, they might not interfere at all with flight and can be kept for no reason,” says Gompel. “The adaptive value comes later.”

This could explain why the helmets have diversified so quickly, evolving their peculiar shapes in less than 40 million years. There is no way that legs or wings could change so quickly – they have important jobs to do and they’re constrained in how they can vary. Without such constraints, the early helmets were free to explore different shapes. This is all fairly speculative, and Gompel is going to explore these issues in future studies.

Partly, these are difficult questions to address because no one really knows what the treehoppers do with their helmets today. The most common answer, although no one has formally tested it, is disguise. “Their shapes are reminiscent of elements found in the wild, including thorns, caterpillar or bird droppings, leaf debris, seeds and even an ant in aggressive posture,” says Gompel. “Of course this is all human interpretation and there is a need to test the real adaptive value and function of these shapes.”

He also suggests another more intriguing possibility. “These animals communicate a lot by sound. It is conceivable, but again not tested, that the hollow helmet is a sound amplification device.”

Reference: Prud’homme, Minervino, Hocine, Cande, Aouane, Dugour, Kassner & Gompel. 2011. Body plan innovation in treehoppers through the evolution of an extra wing-like appendage. Nature

* These genes have strange names because of a tradition among geneticists who study fruit flies. They name their genes based on what the flies look like when the genes in question are switched off. Hence: bazooka, escargot, lava lamp, etc.


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