Insects with three pairs of wings?

Different animal groups are characterized by a stable morphological organization, or body plan. For instance, insects have 3 pairs of legs and up to two pairs of wings. We have found a group of insects, treehoppers, where this body plan has changed with the gain of a novel wing-like appendage.

HFSP Career Development Award holder Nicolas Gompel and HFSP Long-Term fellow Jessica Cande and colleagues
authored on Tue, 03 May 2011

Historically, developmental biologists got interested in morphological evolution by trying to understand how body plans, which describe the basic anatomical organization of groups of animals (e.g., vertebrates, insects, etc.), are assembled and how they evolve. They found that while various body plans are built using similar genetic components, the arrangements and function of these components are too divergent to illuminate body plan evolution: the differences are too numerous and happened too long ago to reconstruct the precise evolutionary path from one form to another. The evolution of body plans, in particular the addition of novel features, is therefore still poorly understood.

To tackle the question of body plan evolution we are studying a group of insects, the treehoppers (Membracidae), which, we submit, have evolved a novel thoracic appendage, and thereby depart from the typical winged insect body plan. The presence of dorsal flight appendages on the second (T2) and third (T3) thoracic segments is a hallmark of the winged insects body plan. Treehoppers, in addition to T2 and T3 wings, have acquired a novel dorsal structure named the helmet, which derives from the T1 segment. In order to trace the evolutionary origin of the helmet, we have gathered anatomical and gene expression data describing the formation of this morphological novelty. Anatomical observations show that the helmet is a dorsal appendage, rather than a mere extension of the T1 segment, and that it shares multiple structural similarities with wings. Furthermore, the helmet’s development uses the same genetic programme that underlies the patterning of wings. Altogether our data indicates that the helmet is a fused pair of modified wings on T1, making the treehoppers the only known group of extant insects equipped with three pairs of wings, and therefore a derived body plan.

With the exception of segments T2 and T3, the genetic programme of wing development has been maintained repressed by Hox genes in all insects for 300 million years. We have found that in treehoppers, this genetic programme has escaped Hox repression in T1, leading to the expression of genes directing the formation of a pair of (modified) wings on T1. Overall, this example uncovers how a novel morphological structure, leading to a body plan modification, has evolved by changing the regulatory response of a genetic programme to a repressive Hox input shared by all insects.

Reference

Body plan innovation in treehoppers through the evolution of an extra wing-like appendage. B Prud’homme, C Minervino, M Hocine, JD Cande, A Aouane, HD Dufour, VA Kassner and N Gompel. Nature, DOI: 10.1038/nature09977, 5 May 2011.