From 250 million years of repression, a wonderland of hats

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

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 http://dx.doi.org/10.1038/nature09977

* 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.

Comments (17)

  1. Whoa! This paper looks to be an instant classic.

  2. Wow, those species that look like ants are *incredible* mimics!

  3. Robert S-R

    I’m a fan of natural selection’s endless supply of creativity. : )

  4. Fantastic piece of work there Ed!

  5. Greg Z.

    “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.”

    Some extinct and fossil insects had prothoracic lobes, but were they really wings?

  6. Is runaway sexual selection not a possible explanation for the evolution of these stunning features? Surely more probable than the “Without such constraints, the early helmets were free to explore different shapes” proposal.

  7. easy to test the sexual selection hypothesis, afaik its only the males who have extravagant displays

    or if you really want to test it, get 10 females, 10 males, 10 males with the helmets either partially cut off or painted over and 10 males with prosthetic larger helmets. Now see which 10 males get sex

  8. Dan Smith

    I wonder what the closest outgroup is (cicadas?). Resequencing and a phylogeny would be really interesting. Makes you wonder whether T1 in drosophila could similarly be induced to make helmets when this is understood. The receptiveness to fusion in the helmet primordia is interesting, wings mustn’t fuse & aberrant fusion is a live clinical issue (eg cleft palate, hypospadia).

    Sexual selection would imply sexual dimorphism and likely a fitness cost (I’m so great I can wear an ‘eat me’ hat and survive). I can’t see any reference to this being sex linked in the paper (and it would surely have said). The examples that strongly suggest ant mimicry imply that it is selected for (ants being less palatable and possibly protected by formic acid) but several things may be going on across the group.

  9. Eleanor

    Indeed it does look like the Ascot of the insect world. Didn’t I see Heteronotus at the royal wedding?

    Of course, as the author points out, answering the question “what is the head-gear used for now?” doesn’t really answer the question of “what was it used for then?”. How it arises in the first place is the really tricky bit.

  10. Dan (#8)-

    Membracids apparently emerge from within the enormous family Cicadellidae, the leafhoppers & sharpshooters, although from what I understand, the precise nature of the non-monophyly is not clear enough yet to be able to resolve the taxonomic issues. In any case, the best outgroup for comparison will be a leafhopper.

  11. Robert S-R

    I don’t think any of the helmets are really flamboyant advertisements for sex. Even the most extravagant ones look like dead leaves, fungi, or flat-out warning signs to predators.

  12. Wow, the diversity of shapes here is really amazing, the treehopper’s take on an ant is fantastic, all the essential elements of an ant without quite being like an ant, evolutionary art!

  13. Agreed that these look more like predator defence through mimicry or being potentially toxic and unpalatable. Plus I think such insects are more likely to use pheremonal cues for sexual selection, or more obvious signals such as being larger than the other guy. Ornate non-functional appendages seem more the realm of avian and mammalian sexual selection, but I could be wrong. Apart from those cool antler flies does anyone know of strange appendages being the product of sexual selection in insects? Is the handicap principle generally for larger organisms?

  14. “Apart from those cool antler flies does anyone know of strange appendages being the product of sexual selection in insects?”

    http://en.wikipedia.org/wiki/Giraffe_weevil

  15. Cool, I guess I certainly shouldn’t be surprised at insects getting there first with magnificent handicap displays. I study the origins of domestication and insects beat us to that by, oh, around 50 million years too.

  16. Li

    It is very interesting that treehoppers can discard their helmets to escape. I think the bugs would survive without helmets at least in a short time. Has the wing-like appendage regeneration capacity?

  17. A new paper disputes this hypothesis:

    Mikó I, Friedrich F, Yoder MJ, Hines HM, Deitz LL, Bertone MA, Seltmann KC, Wallace MS, Deans AR. 2012. On dorsal prothoracic appendages in treehoppers (Hemiptera: Membracidae) and the nature of morphological evidence. PLoS ONE 7(1): e30137.

    DOI: 10.1371/journal.pone.0030137

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