Moczek in Nature: “The origins of novelty in evolutionary biology”

Clockwise from top left: Cladonota benitezi; Umbelligerus peruviensis; Nassunia binotata; and a nymph of a Cymbomorpha species.

“Treehoppers are insects that would resemble miniature cicadas were it not for the presence of the helmet. This structure appears to reside on top of the animal’s thorax, and extends dorsally, and in remarkably varied ways, to mimic thorns, animal droppings or aggressive ants. Entomologists joke that some treehoppers use their helmets to send signals to their home planet, so other-worldly is their appearance. Helmets are generally thought to aid in camouflage by disrupting the animal’s shape and outline, or by mimicking thorns, animal droppings or aggressive ants and wasps. Understanding the origin of helmets and other complex traits is among the most enduring puzzles in evolutionary biology. On the one hand, evolution operates within a framework of descent with modification — everything new must come from something old. On the other hand, structures such as the eye, the wing and the turtle’s shell stand out because they lack obvious correspondence to the old. A new paper in Nature by Prud’homme et al. provide evidence that treehoppers have overcome such suppression to produce their helmets. This addresses the puzzle by connecting a complex and highly diverse trait — the helmet of membracid treehoppers — to its origins in both development and evolution.” See Armin P. Moczek, “Evolutionary biology: The origins of novelty,” Nature 473: 34–35, 05 May 2011, which refers to Benjamin Prud’homme et al., “Body plan innovation in treehoppers through the evolution of an extra wing-like appendage,” Nature 473: 83–86, 05 May 2011.

“Helmets have been interpreted as an extension of the pronotum, the dorsal portion of the first segment of the three-segmented thorax shared by all insects. We have long known from fossil evidence that insects arrived at this organization following a period of progressive loss of wings or wing-like appendages from all abdominal segments, as well as from the first thoracic segment. Fossils of an extinct species (Stenodyctya lobata) show that expression of the wing-development program in the first thoracic segment (arrow) was common in early insects. In extant winged insects, wings are borne only on the second and third thoracic segments, with wing development on the first segment being suppressed.

Enter the treehopper Publilia modesta and its helmet. Through careful analysis of this structure’s anatomy, placement and attachment to the thorax, Prud’homme et al. discovered that the helmet may not be a mere extension of the pronotum. Instead, it is attached bilaterally to the thorax by paired articulations reminiscent of joints, much like regular wings. Moreover, when they examined its early developmental stages, the authors found that the helmet forms from paired buds — again, much like wings. The expanding buds subsequently fuse along the midline, creating the continuous helmet. Study of the expression of one gene, nubbin, normally specific to insect wing development, and two genes specific to appendage formation in general, provided additional evidence that helmet development may rely on developmental mechanisms involved in the formation of wings.

Combined, these observations suggested that treehoppers evolved a way to develop a wing-like structure using a developmental program shared by traditional wings, but in a place in which wing development is typically inhibited in modern winged insects. Prud’homme and colleagues’ investigation of Scr revealed that the gene is still expressed in the prothorax of treehoppers and is able to repress wing formation when transformed into Scr-deficient fruit flies. This implies that wing development in the first thoracic segment of treehoppers was not made possible simply by the loss of the inhibitory ability of Scr, but through some unknown mechanisms operating downstream.

The study by Prud’homme et al. is noteworthy for several reasons. First, it illustrates how, to this day, careful developmental observations can set the stage for startling discoveries. Generations of entomologists have studied treehopper diversity, but research into development has a way of revealing evolution hidden from the study of adults. Second, as with so many studies, it raises as many questions as it answers. Although the morphological observations provide strong evidence that the helmet is a modified wing, the developmental genetic data are modest and correlational: expression patterns can suggest, but not prove, function. And the mechanisms that permit wing-like development in the presence of Scr repression remain to be discovered. Nevertheless, these findings provide a valuable starting point for framing future enquiries into the origin and diversification of the treehoppers’ ‘third pair of wings’.

Finally, and most importantly, the work illustrates how novelty can arise from ancestral developmental potential — how developmental abilities can be lost or silenced over millions of years, only to be redeployed to contribute to the evolution of a complex and beautiful appendage.”

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