Of the winged insects, adults have one or two pairs of wings. During the past 250 million years of insect evolution, there have been no exceptions to this. In a fascinating study, Benjamin Prud'homme, Caroline Minervino, Mélanie Hocine, Jessica Cande, Aïcha Aouane, Héloïse Dufour, Victoria Kassner, and Nicolas Gompel may have found something resembling an exception [Reference Prud'homme, Minervino, Hocine, Cande, Aouane, Dufor, Kassner and Gompel1].
Treehoppers (specifically the family Membracidae) are characterized by a “helmet,” which has been thought to be part of the animal's camouflage (Figure 1). The helmet expands dorsally over most of the body length and has diversified to extremes within the family resembling natural forms ranging from thorns or seeds to animal droppings or aggressive ants. Without their helmets, treehoppers are very similar to cicadas. The helmet has been considered to be an expansion of the pronotum, an outgrowth of the cuticle of the first thoracic segment.
Figure 1: Three examples of the wide variety of treehopper helmets.
The anatomy and evolutionary origin of the helmet remain controversial. Using different microscopy methods, specifically scanning electron microscopy and light microscopy (including confocal), Prud'homme et al. showed that the helmet is attached to the first thoracic segment by a complex articulation. A jointed articulation distinguishes an appendage from a simple outgrowth. They found that the attachment points consisted of thin, non-sclerotized (that is, flexible) cuticle flanked by thicker, sclerotized cuticle. This configuration of flexible and hard cuticle defines cuticular joints that connect appendages to the body. In insects with two pairs of wings, this is the type of joint that connects the wings to the second and third thoracic segments. Because the helmet is attached to the first thoracic segment by jointed articulations, it follows that it is a dorsal appendage of that segment. This was completely unexpected in extant insects!
Unlike most appendages, which are obviously paired, the helmet appears to be a single structure in treehoppers, both in adult and nymphal stages. However, Prud'homme et al. found that the helmet originates from two bilateral primordia that later fuse along the dorsal midline. The helmet is therefore a dorsal appendage of the first thoracic segment with a bilateral origin. Additional anatomical observations made with microscopes suggest that the helmet is a fused pair of wing serial homologues.
If the wings and the helmet are serial homologues, then their development must rely on a shared genetic program. A search for shared molecular signatures revealed that a transcription factor (Nubbin) had a spatial deployment during development that corresponded to that seen in wings. There was also evidence suggesting that the helmet escaped the ancestral repression of wing formation imparted by a member of the Hox gene family, which sculpts the number and pattern of appendages.
So how did this apparent appendage evolve into such a morphologically diverse helmet? Prud'homme et al. convincingly propose that, in contrast to wings, the helmet escaped the stringent functional requirements imposed by flight. If the helmet is accepted as a pair of appendages equivalent to wings, then this will be the exception to a pattern that has existed for 250 million years!
