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Body plan innovation in treehoppers through the evolution of an extra wing-like appendage

Abstract

Body plans, which characterize the anatomical organization of animal groups of high taxonomic rank1, often evolve by the reduction or loss of appendages (limbs in vertebrates and legs and wings in insects, for example). In contrast, the addition of new features is extremely rare and is thought to be heavily constrained, although the nature of the constraints remains elusive2,3,4. Here we show that the treehopper (Membracidae) ‘helmet’ is actually an appendage, a wing serial homologue on the first thoracic segment. This innovation in the insect body plan is an unprecedented situation in 250 Myr of insect evolution. We provide evidence suggesting that the helmet arose by escaping the ancestral repression of wing formation imparted by a member of the Hox gene family, which sculpts the number and pattern of appendages along the body axis5,6,7,8. Moreover, we propose that the exceptional morphological diversification of the helmet was possible because, in contrast to the wings, it escaped the stringent functional requirements imposed by flight. This example illustrates how complex morphological structures can arise by the expression of ancestral developmental potentials and fuel the morphological diversification of an evolutionary lineage.

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Figure 1: Morphological diversity in treehoppers is conveyed by the helmet.
Figure 2: The helmet is a T1 dorsal appendage with a bilateral origin.
Figure 3: Wing-patterning genes are expressed in the developing helmet.
Figure 4: Scr and the evolution of T1 appendages.

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Acknowledgements

We are grateful to G. Moraguès for inspiring the project and the loan of specimens. We thank S. B. Carroll for discussions and support during the early stage of the project; M. Morgan and S. Morgan for access to their field property; J. P. Chauvin for assistance with SEM; S. McKamey and C. Dietrich for help with bibliography; D. Milo for discussions; and D. Andrews, M. Averof, S. B. Carroll, A. Kopp, A. Salzberg and Y. Tomoyasu for sharing reagents. We used FlyBase for information support. We also thank F. Leulier, T. Lecuit, M. Averof, C. Desplan and S. B. Carroll for comments on the manuscript. This work was supported by a EURYI award, a Human Frontier Science Program Career Development Award and the CNRS. J.D.C. was supported by a Human Frontier Science Program Long-term fellowship.

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Authors and Affiliations

Authors

Contributions

B.P. and N.G. conceived the project and designed the experiments; B.P., H.D.D., N.G. and V.A.K. collected Publilia specimens; B.P., C.M., J.D.C. and V.A.K. performed cloning; C.M., J.D.C., M.H. and N.G. did the immunostaining; and J.D.C., B.P. and N.G. carried out fly transgenesis and genetic experiments. A.A. made the histological sections, which were analysed by B.P. and N.G. N.G. and M.H. shot images and movies. N.G. made the anatomical dissections and observations. All authors participated in data analysis. B.P. and N.G. wrote the manuscript.

Corresponding authors

Correspondence to Benjamin Prud’homme or Nicolas Gompel.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-9 with legends, Supplementary Table 1 and additional references. (PDF 5347 kb)

Supplementary Methods

The file contains Supplementary Methods and additional references. (PDF 103 kb)

Supplementary Movie 1

The movie shows flexibility of the helmet. The helmet of a living specimen of Publilia modesta is moved by the experimenter. The specimen is glued to a microscope slide by its helmet in the first part of the movie and then held with forceps. Note how the helmet returns to its initial position when relaxed, as a wing would. Also note how the wings are concealed under the helmet cavity. (MOV 13596 kb)

Supplementary Movie 2

The movie shows unfolding of the helmet upon emergence. The last (fifth) nymphal stage of a Publilia modesta specimen is emerging into an adult.The wings unfold first, as any insect wing would, presumably under the pressured hemolymph that the animal pumps into them. Then, the helmet unfolds likewise to completely cover the animal. The other specimen in the movie did not emerge successfully and remained caught in its nymphal shed. After the unfolding of all the dorsal appendages is complete the animals acquire their pigments. The entire process lasts about one hour. This video is accelerated 20 times. (MOV 12038 kb)

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Prud’homme, B., Minervino, C., Hocine, M. et al. Body plan innovation in treehoppers through the evolution of an extra wing-like appendage. Nature 473, 83–86 (2011). https://doi.org/10.1038/nature09977

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